Sensory Systems/Bats

Introduction
The order of bats (chiroptera), which is made up by the suborders of microbats (microchiroptera) and megabats (megachiroptera), are the only mammals that possess the ability to actively fly. This aerial lifestyle, coupled with the fact that bats are mostly active during the night, brings with it the necessity for a sensory system that is very different from that of mammals living and walking on land. It is important that bats can spot objects that are in their way to not fly into them. Additionally, bats must be able to find the prey they hunt and predators that could become dangerous to them in the dark. This means that while most mammals rely mostly on their vision for movement and navigation, bats do not rely only on their eyes to scan their surroundings. Many bats navigate relying heavily on their auditory system, as they use echolocation, or biosonar, to detect objects. But these bats do not only rely on their auditory sense. In fact, they understand their environment through a combination of echolocation and vision, as well as other senses. This combination of echolocation and vision for movements is not used in all bats, as all megabats (with the exception of Rousettus) and some microbats do not possess the ability to echolocate, but rely on vision and other senses, as well as their memory for navigation and object recognition.

Animals use echolocation by producing sounds and interpreting the returning echoes that occur when the sound waves hit objects. Most animals use echolocation to locate other animals, such as prey or predators. Additionally, animals can detect objects in their surroundings with the help of echolocation and move around these objects.

But echolocation is not only used by bats. Many birds, such as cave swiftlets, also possess the ability to echolocate. Echolocation is not only useful for animals that can fly, but is also used by many animals living in the sea and by some nocturnal land mammals, such as shrews and rats. Some mammals and fish living in water, for example dolphins and whales, echolocate, as sound travels efficiently and over long distances in water, and relying on vision is often not possible in the darkness and vastness of the ocean.

The Auditory System of Bats: Echolocation
As explained in the introduction, echolocation is mostly used when vision is not effective, for example in the dark or in water. The animal produces a sound, and then receives and interprets the echoes that return from objects. The outgoing pulse is then compared with the returning echo, and this information is used by the brain to produce an image of the objects in the animal’s surroundings. As there are many different bat species, there are many different echolocation strategies, although all strategies have similar underlying mechanisms.

Very good hearing is necessary to be able to process sounds during echolocation. Bats even hear frequencies in the ultrasonic range above 20kHz, which is far beyond the human range. This is also the range in which they emit the sounds used for echolocation. The very high ultrasonic frequencies are reflected not only by big obstacles, but also by small targets such as insects. This makes them very useful for bats when hunting.

A Short History of Echolocation
In 1793, Lazzaro Spallanzani found out that if he took away the sense of vision by blinding bats, they could still move around obstacles. A year later, Charles Jurine observed that if the auditory sense was taken away, bats flew into objects. These two experiments led to the believe that bats somehow “see” with their ears instead of their eyes. The term “echolocation” was first used by Donald Griffin in 1938, when he detected the ultrasonic sounds produced by bats via a microphone. In the following decades, the principle of echolocation was found to be used in other animals, for example in dolphins.

Ear Anatomy
The ears of echolocating bats have a similar anatomy to those in most other mammals. Their outer ear has a very large pinna to be able to detect incoming sounds from echolocation, and some bats even use the pinna to actively listen for sounds emitted by predators or prey. The tragus, a flap of skin in the external ear, is used to interpret the direction of an incoming echo during echolocation. The ear canal of bats, the tympanic membrane, the three middle ear bones and their cochlea have a similar structure to most mammals, including humans. The cochlea in the bat’s inner ear is covered by sensory cells, which connect to the brain via the auditory nerve. When sound waves enter the cochlea, the sensory cells convert the resulting vibration into neural signals and pass them to the auditory neurons to be transmitted to the brain. A recent study has found the anatomy of the inner ear of bats, namely the wall structure of the ganglion canal around the ganglion neurons, to be connected to their ability to use echolocation and to the frequencies they use for echolocation.

Sound Production and Propagation
Bats produce sounds via a continuous emission of high-frequency, ultrasonic sound waves produced in their larynx. These sounds are then emitted through the animal’s mouth or nose, depending on the bat species. Many bats can vary their calling rate depending on what they are calling out for, and different species of bats produce signals with different frequencies across the duration of the sound. The produced sound waves are then carried in all directions through the air in the form of sound pulses, as is shown by the orange wave in Figure 3.

Echo Reception and Sound Processing in Ear and Brain
If the sound waves released by the bat come into contact with an object, some of the waves are reflected, as is shown by the green wave in Figure 3. The incoming echo is received by the bat via their relatively big ear flaps, the pinnae. When receiving the echo, bats can extract information about the size, distance, shape, and texture of the object.

The time delay between the production of a call and the reception of the returning signal is measured to find the distance to an object. The vertical direction of an object is found via interpretation of vertical angles, which in bats is done using the tragus. The horizontal direction is determined by differences in the sound intensity received in each ear. The size of an object can be determined via the strength of the echo, and the peaks and troughs in the frequency spectrum of the echo give cues about surface texture. Effects such as the Doppler effect, as well as different pitches during sound production, also help bats detect the distance between them and a detected object. The bat’s auditory nervous system processes the information received by the ears and a mental map of the bat’s surroundings is constructed in the bat’s brain. The bat can thus avoid obstacles and predators and locate prey using echolocation.

During their evolution, bats have developed a “send-receive-switch” system. When they produce their very loud calling sounds, the receiver function is disconnected momentarily to make sure it is not damaged by the loud sound, and then connected again to receive the returning signal, which separates the call and echo in time. This switching is done via middle ear muscles attached to the bones of the inner ear. When a bat emits a loud sound, these muscles contract, and the bones cannot transmit sounds well, leading to sounds not being received while the muscles are contracted, which is an active reflex in humans as well. Most bats only make another call once echoes from the last call have been received, as this makes sure the outgoing and incoming waves do not disrupt each other.

The Role of Echolocation in Hunting
As mentioned before, bats continuously emit sound pulses and interpret echoes in real time, to be able to change their flight speed and trajectory very fast to move around objects. But this is not all echolocation is helpful for. While echolocation is mostly used for orientation during movement, it can additionally be useful for detection and classification of prey and predators. Some bats can even adjust the frequency of their calls depending on the circumstances, for greater hunting efficiency and adaptability.

When on a routine flight, bats produce about 5 to 10 calls per second, and when prey, such as an insect, is located, the calling rate will increase to find the exact location of the insect, and can reach up to 200 calls per second. A noctule bat hunting insects for example will thus use relatively long narrowband signals to detect prey, and once an insect has been detected, will switch to shorter broadband signals with an increasing calling rate to find the exact localization of the insect, leading to a so-called “feeding buzz”. If an animal or object is still far away, a too high calling rate is not preferable, as outgoing signals can mix with returning signals and lead to wrong interpretation of the object’s location. Additionally, calling also needs a lot of energy, so a lower calling rate is better when no near prey or object has been located.

Vision
Even though most bats use echolocation to understand their surroundings, they also possess the ability to see. Bats are said to have high spatial acuity, sensitivity and even possess the ability for depth perception. They have the best vision in low-light conditions, as they mostly move in the dark. Their vision is mostly black and white, and they only possess limited colour vision.

Touch
While research about the sensory system of bats mostly focuses on the role of echolocation, some studies show that bats have hairs on their flight membranes that act as airflow sensors. This means that bats feel air flow when they fly and can respond to changes in aerodynamic conditions as well as to echoes returning from objects. The hair cells on the wings seem to play a role especially in the adaptation of flight speed. Additionally, bats can use the sense of touch for object detection, which can help them capture prey in situations where echolocation is not effective.

Smell and Taste
The olfactory and gustatory senses are the least important senses for bats. The sense of taste, like in humans, is mostly active when tasting food. The sense of smell is used for identification of possible mates, as well as prey and predator detection. Additionally, bats make use of their sense of smell to communicate.

Multisensory Integration
The combination of vision and echolocation bats use during their flight makes them ideal animals to study multisensory integration. Although this might not be possible for a long time anymore, as bat populations have declined over the last years, leading many bat species to be classified as endangered. Danilovich et al. found bats to use their sense of vision to learn the three-dimensional shapes of objects in their surroundings and when deciding where to fly. Meanwhile, echolocation seems to be more important when approaching an obstacle or classifying an object. They have additionally found bats to be able to translate information received via echolocation into a visual representation in their brain. Not only vision and hearing are important, as the sense of touch seems to play a role in flight navigation, although the importance of the tactile sense in comparison to the visual and auditory sense is debated.