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This special takes you on a journey in which you can explore the lives and behaviour of European owls, from hunting to food processing and from migration to conservation. The basis is formed by comparisons of external and internal morphology, linked to physiology and behaviour, which is used to explain ecological differences between owl species. It goes beyond the commonly known owl adaptations, based on novel data analyses derived from newly performed dissections. What is commonly considered as an ‘owl characteristic’, is often not applicable to all owls, but dependent on the current state of a species’ evolution, arisen from the interplay between evolutionary relationships and ecology.

Senses

Hearing
The more an owl hunts upon hearing, the more specialised or adapted hearing features are generally needed. This also goes for owls hunting invisible prey, like voles under snow cover, which can be considered similar to hunting in the dark. Just like humans, owls have two ears, a left and right – but what is the purpose of having two ears? This can be explained using the figure below. If a sound is perceived from a certain direction, for example from the right of where the owl is, the right ear will pick up the sound slightly faster than the left ear.

Now, owls have some highly specialised adaptations in both internal and external structures of their ears, some of which are closely related to the ancestral relationships between species. All these morphological features and the degree to which they are developed play a role in the hearing capacity of owls and will be discussed next. 

• Asymmetry
  The second feature is the functionality of asymmetrical ear slits, as mentioned before, which can have different types and which seems to depend on evolutionary and functional drivers. In Barn Owls, for instance, a slight degree of asymmetry in the height of the ear opening is present in the skin, whereas Tengmalm’s Owls show an extreme example of asymmetrical ear openings in the skull (photo; red circles). Both species heavily rely on their hearing to hunt and use functional ear asymmetry to do so, but in different manners. This is likely a result of their relatively large unrelatedness, evolutionary-wise.

• Skin flap
  Another feature is the skin flap found in some owls. Especially Asio owls, like the Long-eared and Short-eared Owl, have highly developed flaps in front of and behind their ear openings. Other owls can have (one or two) smaller skin flaps in a variety of shapes and sizes, like the Ural Owl here and most other Strix owls. The front skin flap covers the ear opening and is fringed with a fan of open-structured feathers, which together with the skin flap cancel direct noise from entering the ear opening. Hence, the hearing is not disturbed by direct, loud noises but can be focused on high-pitched prey cues instead. Owls that are less dependent on hearing – mainly diurnal eyesight hunters – can lack a skin flap completely, of which the Northern Hawk Owl is an example. 

Although Barn owls are strictly nocturnal hunters, they seem to have relatively small ear slits given their position in the graph (red circle). Looking at more aspects of their ears in an integrated way it becomes apparent that their ears look quite different than in all other owls.

The ear slits of Barn Owls have a very distinctive, almost rectangular shape and a skin flap as seen in no other owls, covering the front of the ear to filter out direct sounds, making them still highly specialised in nocturnal hunting upon hearing. An explanation could be that Barn Owls belong to another owl family than all other owls studied here. Given that, it is most likely that their unexpected position is a result of the different phylogenetic backgrounds, resulting in a different ear structure that is not fully comparable with owls from the other family. The example above underlines that morphological features should be treated in an integrated way with the lifestyle and evolutionary background of species taken into account.

Owl hearing in a nutshell
Owls are unique in showing a wide array of morphological hearing adaptations, of which the main features are: 1) large ear slit size, 2) asymmetrical ears, 3) skin flaps around the ear slit and 4) a facial ruff. The degree to which each of these adaptations are developed and the combination of them results in a sort of ‘hearing toolbox’, indicating how well an owl is specialised in hunting upon hearing. These tool sets vary quite a lot between species and relate to factors as the time of day an owl hunts, the hunting strategy, the type of prey and the environment an owl lives in. Prey can be invisible to the eye due to darkness, but also as a result of vegetation or snow cover. In that regard owls (and raptors like Hen Harriers) hunting in daylight face the same challenge in prey detection as nocturnal hunters.
Overall conclusion: the most specialised ears are found in owls hunting visibly hard-to-detect prey, regardless of their evolutionary relatedness or of being nocturnal of diurnal.

Eyesight
The hearing adaptations mentioned above offer owls a unique and very specialised hunting technique in the dark. However, they do take up much space around an owl’s head, which leads to certain limitations in the owl head morphology. Especially the facial disk and skin flaps would block a large part of an owl’s view if the eyes would be positioned on the sides of the head, like in birds of prey and other birds (left), restricting the field of view significantly (red triangle). Instead, owls have their eyes positioned towards the front, resulting in a binocular and much less restricted view (right).

Most probably, this is the result of the highly developed hearing adaptations, forcing the eyes to change position over time through evolution. In comparison, from the perspective of diurnal birds of prey there is no need to place the eyes in front of the head as their hearing apparatus is far less developed.

So, it seems that owl heads are broad in order to fit both an extensive hearing system and large eyes in the skull. To find out if the hearing system caused the eyes’position to have changed in owls, we take a look at the orientation of eyes in other nocturnal birds. An example are frogmouths, which hunt insects and small vertebrates upon eyesight at night and lack specialised hearing features.

When comparing the skulls of a frogmouth (left) and an owl (right) from above, it becomes clear that the angle at which the eyes are placed in the skulls is quite different. It also shows that the wide skull of frogmouths is clearly not a result of the orientation of the eyes, but of the wide beak instead, enabling them to catch and swallow large prey. This comparison suggests as well that the hearing adaptations of owls indeed seem to have resulted in a more forward-facing orientation of their eyes.

Owls even sacrifice part of their resolution in order to see better in low-light: their eye rods, photoreceptor cells in the eye retina, are bundled (indicated in red in figure). Bundling the eye rods lowers the threshold of light needed to send a single signal to the brain. This results in a lower amount of light needed to perceive a view and therefore helps owls to see in dim light. As a consequence, the total number of rod signals creating an image is relatively low in owls, resulting in a low resolution (low sharpness). In contrast with owls, in diurnal raptors every individual eye rod transfers a signal to the brain (figure), resulting in a much higher resolution.

Another brain-related feature of the eyesight of owls is that their hearing nerve branches off to the optical centre (tectum opticum) before it continues to the audio centre of the brain. The dashed yellow line in the figure indicates how this should be organised in the owl’s brain.

This suggests that owls might be able to create a visual perception of where audio cues are located! In other words, they could be able to “see” where sounds come from in their environment. This can be imagined as looking over a forest patch (photo), in which the owl does not see a mouse – even in daylight – but it does “see” where the sounds of the mouse are coming from, both in light and pitch dark conditions.

Owl eyes in a nutshell
Owl eyes seem to be positioned in a binocular orientation as a result of creating space for specialised hearing adaptations. This forces owls to turn their heads in order to point their ears and eyes for orientation. Owls have a larger number of vertebrae than humans, allowing them to spin their necks quite far – obscured by a thick layer of feathers – and therefore keeping their head-turning myth alive. Owl and raptor eyes are both very large, but for different reasons: owls need large eyes to catch enough light in dim light, whereas raptors need the size to create a sharp view. Owls even sacrifice part of their resolution in order to improve vision in low-light by bundling rod cells in their eye’s retinas. Part of the audio information of owls is processed in the visual centre of the brain, suggesting that owls may be even more specialised by “seeing” where sounds come from in their environment.

Flight
Owl feathers are unique because of a distinctly soft and fluffy texture on the surface of most feathers and hair-like structures on the inner vane of their flight feathers. The leading edges of the outer primaries also have a comb-like row of barbules, called serrations, which aid in silent flight (photos below). The main function of these serrations is to force the air layer flowing over the wing to stick to the wing surface better, retaining the so-called laminar flow and minimizing the air drag over the wing. Drag along the wing causes noise, so lowering the drag also reduces noise produced by the owl’s flight.

These examples (A-F) indicate that owl species hunting in-flight by using their hearing system to catch prey tend to have higher developed serrations and fluffy wing surfaces (D, E, F) compared to species that hunt by foot (A) or upon eyesight (B, C) to quite some degree. Owls that depend on their hearing for either nocturnal hunting or diurnal hunting probably both benefit from the serrations as they aid in minimizing noise in flight.

Another aspect enables most owls to have a silent flight: a low wing loading. This means that the body mass carried by the wing surface is relatively low, or in other words, the wing surface is relatively large for the body mass. A low wing loading allows a slower flight speed, which in turn produces less noise than a fast flight as a result of limited air drag and wing flapping. So, the relatively large wings of owls contribute to noise reduction by allowing slow flight!

Secondly, many birds of prey spend long periods soaring in the air in search of prey, for which a low wing loading is very convenient as it minimizes the energy needed to fly. Another important factor for raptors that hunt by pursuing their prey, like some harriers (photo below) or Sparrowhawks, is that large wings provide a high manoeuvrability. A large wing surface allows them to change their course radically when the wings are twisted or turned. This means that a low wing loading can have several functions, depending on the type of hunting and lifestyle of the bird.

A low wing loading can also work for owls that hunt using high-speed flights, like Short-eared Owls, which need to manoeuvre fast in order to respond to prey cues in time in order to have success. The movements of the wings are powered by the flight muscles.

The advantage of comparing the size of the breastbone keel between species instead of the flight muscle itself is that muscle sizes vary with condition and breastbones do not. Compare the flight muscles of an owl in poor (left) and good (right) condition below.

When zooming in on owls as a group, the flight muscle size appears to be highly variable. A logical expectation would be to find larger flight muscles as wing loading increases, because larger wings generally need larger muscles to control them. The graph below shows the relationship among owls between wing loading and flight muscle size (expressed in keel size), corrected for their body size. The line indicates the “average” relationship between the two characteristics for all European owls. Owls above the line have relatively large flight muscles for their size; owls below the line have relatively small flight muscles.

This graph shows that species that are very closely related and seemingly very similar, actually can be positioned on two extreme ends of the graph, like two species of the Asio genus: Long-eared Owl and Short-eared Owl. Short-eared Owls hunt open grasslands at high speeds with high manoeuvrability and also migrate over long distances, for which strong flight muscles are needed. On the contrary, Long-eared Owls are more of using a sit-and-wait and slow flight technique in denser habitats and have less need for migratory performances.

In fact, the variation between these related species is much larger than between unrelated species from other genera! The comparison between both Asio species shows that similarities develop as a result of ecological relevance, regardless of evolutionary (un)relatedness of species. This example shows very clearly that evolutionary relatedness is not per definition leading in morphology.

In addition to the surface area and flight muscles, the wing shape is a third factor influencing the flight performance of owls. The wing shape can be defined by the aspect ratio, which is a measure of how slim the wing is. The higher the aspect ratio, the slimmer the wing. Slimmer wings are more efficient as a result of reduced wind drag in flight, but require stronger (heavier) wing bones due to their length. So, why wouldn’t all owls have very long, slim wings? 

Because long wings can be very inconvenient for certain habitats or flight types: imagine a forest-dwelling owl flying through a dense forest with very long wings.

Owl flight in a nutshell
Most owls, especially species hunting at night or in densely vegetated habitats, need to fly silently in order to minimize the noise hindering them from hearing prey. They can do so thanks to fluffy feathers and serrations and a low wing loading, which keep their drag and thus noise low. The wing shape is also an important factor determining flight performance. Alltogether, a large variety is present among owls regarding flight adaptations, most of which can be related to the different hunting techniques and lifestyles that different owls have. Diurnal raptors can share owl adaptations, but generally use them for different reasons that relate to their different lifestyles.

Prey capture

Legs
At first sight owls seem to have relatively short legs compared to most diurnal raptors. The main reason for this impression is the thick layer of feathers covering the body of owls, making their legs almost invisible on the outside. When looking under that cover of feathers, however, it turns out that the length of the legs is not that different between owls and raptors overall (graph). Although raptors are generally larger and heavier than owls, placing them higher in the graph, their relative leg length can be considered similar to that of owls: all dots roughly follow the same line in the graph. Here, we compare the lengths of the lower leg, made up of the shinbone and the tarsometatarsus, hereinafter referred to as shinbone and tarsus. No clusters can be distinguished for total lower leg length. 

Remarkably, when comparing the shinbone and tarsus lengths with each other, two groups can be distinguished among both owls and raptors (blue lines in graph). This means that the shinbone length is variable, whereas the length of the tarsus bone remains quite consistent with body size. This leads to the question what the purposes of a longer shinbone might be.

A longer shinbone results in a longer leg, which might be useful for owls hunting in tall vegetation, although having a longer tarsus might be more helpful. A more logical purpose of the shinbone is muscle attachment: the leg muscles operating the tarsus and the toes are positioned on the shinbone. This means that a longer shinbone might offer more space for leg muscles to attach to and therefore result in a more powerful grasp.

The graph below shows that for example Snowy Owls, Ural Owls and Eurasian Eagle Owls have relatively long shinbones. How does that relate to the lifestyles of these owls? It could be related to the large prey they are known to hunt and the grasp needed to kill and transport the catch.

Turning toe
A well-known feature of owls is the ability to twist their lateral toes backwards, often referred to as their so-called turning toe. When at rest, the lateral toe is positioned forwards together with the central and inner toe (A). When twisted backwards, two toes point forwards and two backwards, creating a cross-shaped foot arrangement called zygodactyl feet (B). The idea behind this feature is that owls can enclose smaller prey better with talons arranged this way.

When zooming in upon the variation of the ability to twist the toe backwards among owls, it becomes clear that differences can be significant, both between and within genera. Tawny Owls and Ural Owls, for instance, can turn their toes backwards up to an extreme angle, whereas Eurasian Eagle Owls are much more restricted in turning their toe back, and even resemble diurnal raptors in this sense (graph). Owls that generally catch small prey, like Little Owl and Eurasian Scops Owl, also seem to benefit from this adaptation. Therefore, the size of prey – or the need to hunt opportunistic – is most likely the explanation for the functionality of having a well-developed turning toe.

For species that exclusively hunt small prey, like voles, it can be very beneficial to have talons fully enclosing a victim. For species hunting a large variety of prey types including large prey, like eagle owls, it might be less beneficial. This also means that having an effective turning toe is not strictly related to an owl’s size. The graph also shows two remarkable data points of birds of prey with a very large turning toe angle (encircled red). Which raptors could this be?

Prey capture in a nutshell
The length of the shinbone is quite variable among owls, in which long bones can provide more space to attach leg muscles on to. More muscles represent a higher muscle force an owl can deliver when grasping prey or when reaching through snow layers, resulting in long leg bones to be found in owls in need of relatively much muscle power. The typical turning toe is found to be well-developed in owl species hunting small prey. It can even be found in a diurnal raptor species: Osprey use a highly developed turning toe in order to grasp fish in flight!

Prey processing

Mouth
As a first step the prey must be swallowed in order to start the digestion process. Owls have a relatively wide mouth relative to their size compared to raptors (graph), which allows them to swallow their prey whole. One might think that this is an adaptation that specially evolved to process large prey, but that is not the case. To explain how this feature actually developed we compare owls to nightjars, which are nocturnal aerial hunters that also have wide mouths for their size (blue dots), which they use to collect insects in flight.

Taking a look underneath the skin of these birds we can quite easily tell what causes them to have a wide mouth: owls have broad heads and mouths accordingly as a result of their very big eyes, forcing the skull to expand to the sides (drawing A).

In nightjars, however, the size of the beak determines the width of the skull (drawing B). In both skulls the brain did not expand with the size of the skull and additional spaces resulting from this shape are filled up by spongy bone tissue. So, in nightjars the size of the mouth and in owls the size of the eyes seems to have determined the size of their head.

For many owls, having a wide skull – and therefore a wide beak – resulted in the luxury to swallow prey whole. Consequently, swallowing big prey whole might have resulted in the lack of a crop in owls, as prey of that size may be too big to store in it. Raptors do have a crop, in which they store ripped-off pieces of their prey, ingesting it bit by bit. Larger owls or owl species catching relatively large prey also first dismantle their catch before ingesting it, similar to birds of prey.

Digestive system
After swallowing (and lacking a crop), food items run through the oesophagus and enter the stomach, of which the size also seems to relate to the prey (partical) size that owls eat. Larger species like Eurasian Eagle Owls, which dismantle their prey and swallow it in pieces, show stomach sizes comparable with those of diurnal birds of prey. Medium and smaller owls like Barn Owl or Little Owl, however, have relatively large stomachs compared to diurnal raptors of similar size, which allow them to store a fair number of larger prey. These can be rodents, birds, insects or even worms and spiders, depending on the species (here a Tawny Owl stomach filled with earth worms).

The actual digestion starts in the stomach, where acidic fluids and digestive enzymes are added to the content. Then it passes through to the intestine, which is relatively short in owls, just like in most other carnivorous birds. The variation in intestine length among owls appears to be very small. Owls, however, do have an adaptation in their digestive system unlike diurnal raptors: caeca (blue arrows).

Caeca are blind guts, dead-end tubes in which bacteria process waste products, connecting at the end of the small intestine. These waste products are uric acids from the kidneys, which are transported from the cloaca back into the caeca using anti-peristaltic movements. The bacteria present in the blind guts produce proteins from these uric acids. In turn, the owl can digest the proteins produced by the bacteria, which can make a significant contribution to an owl’s basic energy needs. The ability of owls to use their blind guts as an extra energy source where birds of prey cannot, could make a difference in times of food shortage or affected habitat quality.

The body condition, time of year and sex may all influence the size of blind guts in owls. This results in a large variation of blind gut size within species, which makes it difficult to compare the actual differences in functionality between species. Despite this variation, owls living in tight balance with prey intake or with additional amino acid needs (e.g. for egg production) are expected to have larger blind guts.

Prey processing in a nutshell
The large, forward facing eyes of owls seem to have resulted in a wide skull and, consequently, a wide beak. This allows them to swallow prey whole unlike raptors and may even be the reason for owls to lack a crop. Stomachs of owls are generally large, especially in smaller species, and serve to store large food items whole. The rest of the digestive system shows little variation among owls, although all owls have a unique feature: blind guts. In these guts bacteria process waste products from the kidneys, which can make a significant contribution to an owl’s basic energy needs. The ability of owls to do so could even make a difference in situations of food shortage or affected habitat quality.

Summary

Main findings
This summary gives an overview of the main findings we can derive from this European Owl Special, based on the combinations of owl anatomies and lifestyles:

• Hearing adaptations are a dominant factor in (the origin of) owl morphology, although some owls nowadays show little advanced hearing adaptations
• Owls and birds of prey differ more than would be expected at first sight
• Nevertheless, dependent on size and ecology, some adaptations show some overlap between owls and birds of prey
• Owl species clearly differ, even if closely related, in relationship with ecological differences
• Within a species, characteristics can vary a lot due to individual differences

Owl types
Based on the findings of this special we can make a new classification of European owls, based on their morphology rather than on taxonomical position. Such a classification – based on morphological traits and ecological niches – can be considered an overview of the different types of owls in Europe. As concluded above, the extent to which owl hearing adaptations are developed is a dominant factor in the morphological classification, which distinguishes three groups among European owls:  1) owls with excellent hearing, 2) owls with intermediate hearing and 3) owls with poor hearing.

Eye size is another important factor determining which environment an owl can live and navigate in, because orientation in an owl’s habitat is not possible upon hearing only. For prey detection some owls use their hearing primarily, whereas others mainly rely upon eyesight or use a combination of both senses. The following distinction with respect to eye size can be made:  1) owls with small eyes and 2) owls with large eyes.

A third distinction can be made upon adaptations for flight performance in the sense of wing shape (in relation with habitat) and the breastbone keel size (representing muscle power):  1) owls with long, slender wings and 2) owls with short, broad wings and 1) owls with large breastbone keels and 2) owls with small breastbone keels, respectively.

The combinations of the traits mentioned above summarize how each owl type can detect its prey and which flight performance is needed in order to find the prey, including potential migration. Additional aspects (e.g. shinbone length, habitat and body size) further differentiate niches within the categories made above. A morphological classification as described above results in 9 owl types and 14 different niches – equal to the number of species – meaning that each species seems to fullfill a unique niche!

The figure below shows the morphological distinctions made and the ecological niches resulting from it: each number (1-9) represents such an ecological niche. Interpretation of each niche and additional distinctions within niches are clarified below the figure (legend).

Legend

1. Nocturnal prime eyesight hunters: a slight niche difference among this type is represented by species with flight adaptations supporting migration (Eurasian Scops Owl) against sedentary species with poor flight adaptations (Little Owl). 
2. Migratory diurnal prime eyesight hunters: Snowy Owls are adapted to diurnal hunting and migrate to follow prey fluctuations. They can even be restricted to hunting in complete daylight conditions during midnight sun periods in polar areas.
3. Sedentary diurnal prime eyesight hunters: this type of diurnal eyesight hunters lack the flight adaptations that allow migration (Eurasian Pygmy-owl)
4. Nocturnal hunters using eyesight & hearing: the distinction among this type of owls is primarily body size, which probably also relates to prey size and type that a certain habitat offers. Large species generally require a habitat with larger/more prey, although large species (Tawny Owl) can also exclude smaller species by predating upon the latter (Tengmalm’s Owl). 
5. Nocturnal hearing hunters of open landscapes: these owls show a high overlap in habitat type, but are probably distinguished based on nesting ecology, in which some are cavity nesters (Barn Owl), whereas others depend on trees or abandoned nests of other birds (Long-eared Owl). 
6. Diurnal hearing hunters of open landscapes: this type uses its excellent hearing to hunt prey in densely vegetated areas, because hunting upon eyesight nearly impossible. The ability to migrate can be crucial for this type in order to follow prey fluctuations.
7. Hearing hunters of half-open & forested landscapes: among this type, some owls hunt upon hearing in forested areas (Ural Owl), whereas others roam half-open or taiga habitat (Great Grey Owl), sometimes even using their excellent hearing to catch prey invisible to the eye by snow cover, for which they seem to benefit from long shinbones that provide power and range to reach through the snow. 
8. Eyesight hunters with little hearing adaptations and large eyes: these owls seem to have highly adapted eyes for hunting, and despite being diurnal for a large bit, they also have some hearing adaptations (Northern Hawk Owl).
9. Eyesight hunters with little hearing adaptations and small eyes: this type seems to have the least advanced senses (small eyes & restricted hearing adaptations), but their large size might allow them to catch larger and easier-to-detect prey. Further distinction can be made based on flight performance, related to being highly opportunistic in a challenging habitat (Pharaoh Eagle Owl) or having higher prey densities to the exposal (Eurasian Eagle Owl).

Beyond Europe
Apparently, a large number of owl types is present among European owls, in which all species even seem to fullfill a unique ecological niche. However, a diurnal eyesight hunter of forested areas does not seem to be present among European species. How would this be in other parts of the world? Do owl species fulfill the same niches in other habitats, and do they overlap among species?

In order to answer part of that question, we will be studying the North-American owls soon in order to find out if new niches or owl types can be distinguished!