Animal echolocation
Encyclopedia
Echolocation, also called biosonar, is the biological sonar
used by several kinds of animal
s.
Echolocating animals emit calls out to the environment and listen to the echoes
of those calls that return from various objects near them. They use these echoes to locate and identify the objects. Echolocation is used for navigation
and for foraging
(or hunting) in various environments.
Echolocating animals include some mammals and a few birds; most notably microchiropteran bat
s and odontocetes (toothed whales and dolphins), but also in simpler form in other groups such as shrew
s, one genus of megachiropteran bats (Rousettus
) and two cave dwelling bird
groups, the so called cave swiftlet
s in the genus Aerodramus
(formerly Collocalia) and the unrelated Oilbird
Steatornis caripensis.
The term echolocation was coined by Donald Griffin, whose work with Robert Galambos
was the first to conclusively demonstrate its existence in bats in 1938. Long before that, however, the 18th century Italian scientist Lazzaro Spallanzani
had, by means of a series of elaborate experiments, concluded that bats navigate by hearing and not by vision. Echolocation in odontocetes was not properly described before two decades later, by Schevill and McBride.
, using sounds made by the animal itself. Ranging is done by measuring the time delay between the animal's own sound emission and any echoes that return from the environment. The relative intensity of sound received at each ear as well as the time delay between arrival at the two ears provide information about the horizontal angle (azimuth) from which the reflected sound waves arrive.
Unlike some man-made sonars that rely on many extremely narrow beams and many receivers to localize a target (multibeam sonar), animal echolocation has only one transmitter and two receivers (the ears). Echolocating animals have two ears positioned slightly apart. The echoes returning to the two ears arrive at different times and at different loudness levels, depending on the position of the object generating the echoes. The time and loudness differences are used by the animals to perceive distance and direction. With echolocation, the bat or other animal can see not only where it is going but also how big another animal is, what kind of animal it is, and other features.
s use echolocation to navigate and forage, often in total darkness. They generally emerge from their roosts in caves, attics, or trees at dusk and hunt for insects into the night. Their use of echolocation allows them to occupy a niche where there are often many insect
s (that come out at night since there are fewer predators then) and where there is less competition for food, and where there are fewer other species that may prey on the bats themselves.
Microbats generate ultrasound via the larynx
and emit the sound through the open mouth or, much more rarely, the nose. The latter is most pronounced in the horseshoe bats (Rhinolophus spp.). Microbat range in frequency from 14,000 to well over 100,000 Hz, mostly beyond the range of the human ear (typical human hearing range is considered to be from 20 Hz to 20,000 Hz). Bats may estimate the elevation of targets by interpreting the interference patterns caused by the echoes reflecting from the tragus
, a flap of skin in the external ear. There are two hypotheses about the evolution of echolocation in bats. The first suggests that laryngeal echolocation evolved twice in Chiroptera, once in Yangochiroptera and once in the rhinolophoids. The second proposes that laryngeal echolocation had a single origin in Chiroptera, was subsequently lost in the family Pteropodidae (all megabats), and later evolved as a system of tongue-clicking in the genus Rousettus.
Individual bat species echolocate within specific frequency ranges that suit their environment and prey types. This has sometimes been used by researchers to identify bats flying in an area simply by recording their calls with ultrasonic recorders known as 'bat detectors'. However echolocation calls are not always species specific and some bats overlap in the type of calls they use so recordings of echolocation calls cannot be used to identify all bats. In recent years researchers in several countries have developed 'bat call libraries' that contain recordings of local bat species that have been identified known as 'reference calls' to assist with identification.
Since the 1970s there has been an ongoing controversy among researchers as to whether bats use a form of processing known from radar
termed coherent
cross-correlation. Coherence means that the phase of the echolocation signals is used by the bats, while cross-correlation
just implies that the outgoing signal is compared with the returning echoes in a running process. Today most - but not all - researchers believe that they use cross-correlation, but in an incoherent form, termed a filter bank receiver.
When searching for prey they produce sounds at a low rate (10-20/sec). During the search phase the sound emission is coupled to respiration, which is again coupled to the wingbeat. This coupling appears to dramatically conserve energy as there is little to no additional energetic cost of echolocation to flying bats (Speakman and Racey 1991). After detecting a potential prey item, microbats increase the rate of pulses, ending with the terminal buzz, at rates as high as 200/sec. During approach to a detected target, the duration of the sounds is gradually decreased, as is the energy of the sound.
and Madagascar
, and hunting for food sources as different as insects, frogs, nectar, fruit, and blood. Additionally, the characteristics of an echolocation call are adapted to the particular environment, hunting behavior, and food source of the particular bat. However, this adaptation of echolocation calls to ecological factors is constrained by the phylogenetic relationship of the bats, leading to a process known as descent with modification, and resulting in the diversity seen in the Microchiropteran suborder today. (Jones and Teeling 2006; Grinnell 1995; Zupanc 2004; Fenton 1995; Neuweiler 2003; Simmons and Stein 1980)
One possible disadvantage of the FM signal is a decreased operational range of the call. Because the energy of the call is spread out among many frequencies, the distance at which the FM-bat can detect targets is limited (Fenton 1995). This is in part because any echo returning at a particular frequency can only be evaluated for a brief fraction of a millisecond, as the fast downward sweep of the call does not remain at any one frequency for long (Grinnell 1995).
Additionally, because the signal energy of a CF call is concentrated into a narrow frequency band, the operational range of the call is much greater than that of an FM signal. This relies on the fact that echoes returning within the narrow frequency band can be summed over the entire length of the call, which maintains a constant frequency for up to 100 milliseconds (Grinnell 1995; Fenton 1995)
The basilar membrane
within the cochlea
contains the first of these specializations for echo information processing. In bats that use CF signals, the section of membrane that responds to the frequency of returning echoes is much larger than the region of response for any other frequency. For example, in Rhinolophus ferrumequinum, the horseshoe bat, there is a disproportionately lengthened and thickened section of the membrane that responds to sounds around 83 kHz, the constant frequency of the echo produced by the bat's call. This area of high sensitivity to a specific, narrow range of frequency is known as an "acoustic fovea
" (Schuller and Pollack 1979).
Odontocetes (toothed whales and dolphins) have similar cochlear specializations to those found in bats. Odontocetes also have the highest neural investment of any cochleae reported to date with ratios of greater than 1500 ganglion cells/mm of basilar membrane.
Further along the auditory pathway, the movement of the basilar membrane results in the stimulation of primary auditory neurons. Many of these neurons are specifically "tuned" (respond most strongly) to the narrow frequency range of returning echoes of CF calls. Because of the large size of the acoustic fovea, the number of neurons responding to this region, and thus to the echo frequency, is especially high (Carew 2001).
In the Inferior colliculus
, a structure in the bat's midbrain, information from lower in the auditory processing pathway is integrated and sent on to the auditory cortex. As George Pollak and others showed in a series of papers in 1977, the interneurons in this region have a very high level of sensitivity to time differences, since the time delay between a call and the returning echo tells the bat its distance from the target object. Especially interesting is that while most neurons respond more quickly to stronger stimuli, collicular neurons maintain their timing accuracy even as signal intensity changes.
These interneurons are specialized for time sensitivity in several ways. First, when activated, they generally respond with only one or two action potential
s. This short duration of response allows their action potentials to give a very specific indication of the exact moment of the time when the stimulus arrived, and to respond accurately to stimuli that occur close in time to one another. In addition, the neurons have a very low threshold of activation – they respond quickly even to weak stimuli. Finally, for FM signals, each interneuron is tuned to a specific frequency within the sweep, as well as to that same frequency in the following echo. There is specialization for the CF component of the call at this level as well. The high proportion of neurons responding to the frequency of the acoustic fovea actually increases at this level (Carew 2001, Pollak 1977, Zupanc 2004).
on the mustached bat, Pteronotus parnellii. This bat's call has both CF tone and FM sweep components.
Suga and his colleagues have shown that the cortex contains a series of "maps" of auditory information, each of which is organized systematically based on characteristics of sound such as frequency
and amplitude
. The neurons in these areas respond only to a specific combination of frequency and timing (sound-echo delay), and are known as combination-sensitive neurons.
The systematically organized maps in the auditory cortex respond to various aspects of the echo signal, such as its delay and its velocity. These regions are composed of "combination sensitive" neurons that require at least two specific stimuli to elicit a response. The neurons vary systematically across the maps, which are organized by acoustic features of the sound and can be two dimensional. The different features of the call and its echo are used by the bat to determine important characteristics of their prey. The maps include:
Biosonar is valuable to Toothed whales (suborder odontoceti), including dolphin
s, porpoise
s, river dolphin
s, killer whales and sperm whale
s, because they live in an underwater habitat that has favourable acoustic characteristics and where vision
is extremely limited in range due to absorption
or turbidity
.
Cetacean evolution consisted of three main radiations. Throughout the middle and late Eocene periods (49-31.5 million years ago), archaeocetes, primitive toothed Cetacea that arose from terrestrial mammals with the creation of aquatic adaptations, were the only known archaic Cetacea. These primitive aquatic mammals did not posses the ability to echolocate, although they did have slightly adapted underwater hearing. The morphology of acoustically isolated ear bones in basilosaurid archaeocetes indicates that this order had directional hearing underwater at low to mid frequencies by the late middle Eocene. However, with the extinction of archaeocete at the onset of the Oligocene, two new lineages in the early Oligocene period (31.5-28 million years ago) compromised a second radiation. These early mysticete (baleen whales) and odontocete can be dated back to the middle Oligocene in New Zealand. Based on past phylogenies, it has been found that the evolution of odontocetes is monophyletic, suggesting that echolocation evolved only once 36 to 34 million years ago. Dispersal rates routes of early odontocetes included transoceanic travel to new adaptive zones. The third radiation occurred later in the Neogene, when present dolphins and their relatives evolved to be the most common species in the modern sea.
The evolution of echolocation could be attributed several theories. There are two proposed drives for the hypotheses of cetacean radiation, one biotic and the other abiotic in nature. The first, adaptive radiation, is the result of a rapid divergence into new adaptive zones. This results in diverse, ecologically different clades that are incomparable. Clade Neocete (crown cetacean) has been characterized by an evolution from archaeocetes and a dispersion across the world’s oceans, and even estuarites and rivers. These ecological opportunities were the result of abundant dietary resources with low competition for hunting. This hypothesis of lineage diversification, however, can be unconvincing due to a lack of support for rapid speciation early in cetacean history. A second, more abiotic drive is more supported. Physical restructuring of the oceans has played a role in echolocation radiation. This was a result of global climate change at the Eocene-Oligocene boundary; from a greenhouse to an icehouse world. Tectonic openings created the emergence of the Southern ocean with a free flowing Antarctic Circumpolar current (Fordyce 1980, 2003; Lindberg & Pyenson 2007; Steeman et al. 2009). These events allowed for a selection regime characterized by the ability to locate and capture prey in turbid river waters, or allow odontocetes to invade and feed at depths below the photic zone. Further studies have found that echolocation below the photic zone could have been a predation adaptation to diel migrating
cephalopods. Since its advent, there has been adaptive radiation
especially in the Delphinidae family (dolphins) in which echolocation has become extremely derived.
One specific type of echolocation, narrow-band high frequency (NBHF) clicks, evolved at least four times in groups of odontocetes, including pygmy sperm whale (Kogiidae) and porpoise (Phocoenidae) families, Pontoporia blainvillei
, the genus Cephalorhynchus
, and part of the genus Lagenorhynchus
. These high frequency clicks likely evolved as adaptation of predator avoidance, as they inhabit areas that have many killer whales and the signals are inaudible to killer whales due to the absence of energy below 100 kHz. Another reason for variation in echolocation frequencies is habitat. Shallow waters, where many of these species live, tend to have more debris; a more directional transmission reduces clutter in reception.
Toothed whales emit a focused beam of high-frequency clicks in the direction that their head is pointing. Sounds are generated by passing air from the bony nares through the phonic lips. These sounds are reflected by the dense concave bone of the cranium and an air sac at its base. The focused beam is modulated by a large fatty organ known as the 'melon'. This acts like an acoustic lens because it is composed of lipids of differing densities. Most toothed whales use clicks in a series, or click train, for echolocation, while the sperm whale may produce clicks individually. Toothed whale whistles do not appear to be used in echolocation. Different rates of click production in a click train give rise to the familiar barks, squeals and growls of the bottlenose dolphin
. A click train with a repetition rate over 600 per second is called a burst pulse. In bottlenose dolphins, the auditory brain response resolves individual clicks up to 600 per second, but yields a graded response for higher repetition rates.
It has been suggested that some smaller toothed whales may have their tooth arrangement suited to aid in echolocation. The placement of teeth in the jaw of a bottlenose dolphin, as an example, are not symmetrical when seen from a vertical plane, and this asymmetry could possibly be an aid in the dolphin sensing if echoes from its biosonar are coming from one side or the other. However, this idea lacks experimental support.
Echoes are received using complex fatty structures around the lower jaw as the primary reception path, from where they are transmitted to the middle ear via a continuous fat body (Ketten 1992,2000). Lateral sound may be received though fatty lobes surrounding the ears with a similar density to water. Some researchers believe that when they approach the object of interest, they protect themselves against the louder echo by quietening the emitted sound. In bats this is known to happen, but here the hearing sensitivity is also reduced close to a target.
Before the echolocation abilities of "porpoises" were officially discovered, Jacques Yves Cousteau suggested that they might exist. In his first book, The Silent World
(1953, pp. 206–207), he reported that his research vessel, the Élie Monier, was heading to the Straits of Gibraltar and noticed a group of porpoises following them. Cousteau changed course a few degrees off the optimal course to the center of the strait, and the porpoises followed for a few minutes, then diverged toward mid-channel again. It was obvious that they knew where the optimal course lay, even if the humans didn't. Cousteau concluded that the cetaceans had something like sonar
, which was a relatively new feature on submarines.
s and some species of swiftlet
are known to use a relatively crude form of echolocation compared to that of bats and dolphins. These nocturnal birds emit calls while flying and use the calls to navigate through trees and caves where they live.
and Blarina) of shrews and the tenrecs of Madagascar
. These include the wandering shrew (Sorex vagrans), the common or Eurasian shrew (Sorex araneus), and the short-tailed shrew (Blarina brevicauda). The nature of shrew sounds unlike those of bats are low amplitude, broadband, multi-harmonic and frequency modulated. They contain no ‘echolocation clicks’ with reverberations and would seem to be used for simple, close range spatial orientation. In contrast to bats, shrews use echolocation only to investigate their habitat rather than additionally to pinpoint food.
Sonar
Sonar is a technique that uses sound propagation to navigate, communicate with or detect other vessels...
used by several kinds of animal
Animal
Animals are a major group of multicellular, eukaryotic organisms of the kingdom Animalia or Metazoa. Their body plan eventually becomes fixed as they develop, although some undergo a process of metamorphosis later on in their life. Most animals are motile, meaning they can move spontaneously and...
s.
Echolocating animals emit calls out to the environment and listen to the echoes
Echo (phenomenon)
In audio signal processing and acoustics, an echo is a reflection of sound, arriving at the listener some time after the direct sound. Typical examples are the echo produced by the bottom of a well, by a building, or by the walls of an enclosed room and an empty room. A true echo is a single...
of those calls that return from various objects near them. They use these echoes to locate and identify the objects. Echolocation is used for navigation
Navigation research
Whereas originally the term Navigation applies to the process of directing a ship to a destination, Navigation research deals with fundamental aspects of navigation in general...
and for foraging
Foraging
- Definitions and significance of foraging behavior :Foraging is the act of searching for and exploiting food resources. It affects an animal's fitness because it plays an important role in an animal's ability to survive and reproduce...
(or hunting) in various environments.
Echolocating animals include some mammals and a few birds; most notably microchiropteran bat
Bat
Bats are mammals of the order Chiroptera "hand" and pteron "wing") whose forelimbs form webbed wings, making them the only mammals naturally capable of true and sustained flight. By contrast, other mammals said to fly, such as flying squirrels, gliding possums, and colugos, glide rather than fly,...
s and odontocetes (toothed whales and dolphins), but also in simpler form in other groups such as shrew
Shrew
A shrew or shrew mouse is a small molelike mammal classified in the order Soricomorpha. True shrews are also not to be confused with West Indies shrews, treeshrews, otter shrews, or elephant shrews, which belong to different families or orders.Although its external appearance is generally that of...
s, one genus of megachiropteran bats (Rousettus
Rousettus
Rousettus is a genus of Old World fruit bats or megabats. They are sometimes referred to as dog-faced fruit bats, or flying foxes. The genus is a member of the suborder Megachiroptera...
) and two cave dwelling bird
Bird
Birds are feathered, winged, bipedal, endothermic , egg-laying, vertebrate animals. Around 10,000 living species and 188 families makes them the most speciose class of tetrapod vertebrates. They inhabit ecosystems across the globe, from the Arctic to the Antarctic. Extant birds range in size from...
groups, the so called cave swiftlet
Swiftlet
Swiftlets are birds contained within the four genera Aerodramus, Hydrochous, Schoutedenapus and Collocalia. They form the Collocaliini tribe within the swift family Apodidae. The group contains around thirty species mostly confined to southern Asia, south Pacific islands, and northeastern...
s in the genus Aerodramus
Aerodramus
Aerodramus is a genus of small, dark, cave-nesting birds in the Collocaliini tribe of the swift family. Its members are confined to tropical and subtropical regions in southern Asia, Oceania and northeastern Australia...
(formerly Collocalia) and the unrelated Oilbird
Oilbird
The Oilbird , also known as Guácharo, is a bird found in the northern areas of South America . They are nocturnal feeders on the fruits of the Oil Palm and tropical laurels, and are the only nocturnal fruit eating birds in the world...
Steatornis caripensis.
The term echolocation was coined by Donald Griffin, whose work with Robert Galambos
Robert Galambos
Robert Carl Galambos was an American neuroscientist whose pioneering research demonstrated how bats use echolocation for navigation purposes, as well as studies on how sound is processed in the brain....
was the first to conclusively demonstrate its existence in bats in 1938. Long before that, however, the 18th century Italian scientist Lazzaro Spallanzani
Lazzaro Spallanzani
Lazzaro Spallanzani was an Italian Catholic priest, biologist and physiologist who made important contributions to the experimental study of bodily functions, animal reproduction, and essentially discovered echolocation...
had, by means of a series of elaborate experiments, concluded that bats navigate by hearing and not by vision. Echolocation in odontocetes was not properly described before two decades later, by Schevill and McBride.
Basic principle
Echolocation is the same as active sonarSonar
Sonar is a technique that uses sound propagation to navigate, communicate with or detect other vessels...
, using sounds made by the animal itself. Ranging is done by measuring the time delay between the animal's own sound emission and any echoes that return from the environment. The relative intensity of sound received at each ear as well as the time delay between arrival at the two ears provide information about the horizontal angle (azimuth) from which the reflected sound waves arrive.
Unlike some man-made sonars that rely on many extremely narrow beams and many receivers to localize a target (multibeam sonar), animal echolocation has only one transmitter and two receivers (the ears). Echolocating animals have two ears positioned slightly apart. The echoes returning to the two ears arrive at different times and at different loudness levels, depending on the position of the object generating the echoes. The time and loudness differences are used by the animals to perceive distance and direction. With echolocation, the bat or other animal can see not only where it is going but also how big another animal is, what kind of animal it is, and other features.
Bats
MicrobatMicrobat
The microbats constitute the suborder Microchiroptera within the order Chiroptera . They are most often referred to by their scientific name...
s use echolocation to navigate and forage, often in total darkness. They generally emerge from their roosts in caves, attics, or trees at dusk and hunt for insects into the night. Their use of echolocation allows them to occupy a niche where there are often many insect
Insect
Insects are a class of living creatures within the arthropods that have a chitinous exoskeleton, a three-part body , three pairs of jointed legs, compound eyes, and two antennae...
s (that come out at night since there are fewer predators then) and where there is less competition for food, and where there are fewer other species that may prey on the bats themselves.
Microbats generate ultrasound via the larynx
Larynx
The larynx , commonly called the voice box, is an organ in the neck of amphibians, reptiles and mammals involved in breathing, sound production, and protecting the trachea against food aspiration. It manipulates pitch and volume...
and emit the sound through the open mouth or, much more rarely, the nose. The latter is most pronounced in the horseshoe bats (Rhinolophus spp.). Microbat range in frequency from 14,000 to well over 100,000 Hz, mostly beyond the range of the human ear (typical human hearing range is considered to be from 20 Hz to 20,000 Hz). Bats may estimate the elevation of targets by interpreting the interference patterns caused by the echoes reflecting from the tragus
Tragus
The tragus is a small pointed eminence of the external ear, situated in front of the concha, and projecting backward over the meatus. Its name comes from the Greek: tragos, goat, and is descriptive of its general covering on its under surface with a tuft of hair, resembling a goat's beard...
, a flap of skin in the external ear. There are two hypotheses about the evolution of echolocation in bats. The first suggests that laryngeal echolocation evolved twice in Chiroptera, once in Yangochiroptera and once in the rhinolophoids. The second proposes that laryngeal echolocation had a single origin in Chiroptera, was subsequently lost in the family Pteropodidae (all megabats), and later evolved as a system of tongue-clicking in the genus Rousettus.
Individual bat species echolocate within specific frequency ranges that suit their environment and prey types. This has sometimes been used by researchers to identify bats flying in an area simply by recording their calls with ultrasonic recorders known as 'bat detectors'. However echolocation calls are not always species specific and some bats overlap in the type of calls they use so recordings of echolocation calls cannot be used to identify all bats. In recent years researchers in several countries have developed 'bat call libraries' that contain recordings of local bat species that have been identified known as 'reference calls' to assist with identification.
Since the 1970s there has been an ongoing controversy among researchers as to whether bats use a form of processing known from radar
Radar
Radar is an object-detection system which uses radio waves to determine the range, altitude, direction, or speed of objects. It can be used to detect aircraft, ships, spacecraft, guided missiles, motor vehicles, weather formations, and terrain. The radar dish or antenna transmits pulses of radio...
termed coherent
Coherence (signal processing)
-Background:The spectral coherence is a statistic that can be used to examine the relation between two signals or data sets. It is commonly used to estimate the power transfer between input and output of a linear system. If the signals are ergodic, and the system function linear, it can be used to...
cross-correlation. Coherence means that the phase of the echolocation signals is used by the bats, while cross-correlation
Cross-correlation
In signal processing, cross-correlation is a measure of similarity of two waveforms as a function of a time-lag applied to one of them. This is also known as a sliding dot product or sliding inner-product. It is commonly used for searching a long-duration signal for a shorter, known feature...
just implies that the outgoing signal is compared with the returning echoes in a running process. Today most - but not all - researchers believe that they use cross-correlation, but in an incoherent form, termed a filter bank receiver.
When searching for prey they produce sounds at a low rate (10-20/sec). During the search phase the sound emission is coupled to respiration, which is again coupled to the wingbeat. This coupling appears to dramatically conserve energy as there is little to no additional energetic cost of echolocation to flying bats (Speakman and Racey 1991). After detecting a potential prey item, microbats increase the rate of pulses, ending with the terminal buzz, at rates as high as 200/sec. During approach to a detected target, the duration of the sounds is gradually decreased, as is the energy of the sound.
Calls and ecology
Bats belonging to the suborder Microchiroptera (microbats) occupy a diverse set of ecological conditions - they can be found living in environments as different as EuropeEurope
Europe is, by convention, one of the world's seven continents. Comprising the westernmost peninsula of Eurasia, Europe is generally 'divided' from Asia to its east by the watershed divides of the Ural and Caucasus Mountains, the Ural River, the Caspian and Black Seas, and the waterways connecting...
and Madagascar
Madagascar
The Republic of Madagascar is an island country located in the Indian Ocean off the southeastern coast of Africa...
, and hunting for food sources as different as insects, frogs, nectar, fruit, and blood. Additionally, the characteristics of an echolocation call are adapted to the particular environment, hunting behavior, and food source of the particular bat. However, this adaptation of echolocation calls to ecological factors is constrained by the phylogenetic relationship of the bats, leading to a process known as descent with modification, and resulting in the diversity seen in the Microchiropteran suborder today. (Jones and Teeling 2006; Grinnell 1995; Zupanc 2004; Fenton 1995; Neuweiler 2003; Simmons and Stein 1980)
Acoustic features
Describing the diversity of bat echolocation calls requires examination of the frequency and temporal features of the calls. It is the variations in these aspects that produce echolocation calls suited for different acoustic environments and hunting behaviors. (Fenton 2005; Jones and Teeling 2006; Zupanc 2004; Simmons and Stein 1980; Hiryu et al. 2007)- Frequency Modulation and Constant Frequency: Echolocation calls can be composed of two different types of frequency structures: frequency modulated (FM) sweeps, and constant frequency (CF) tones. A particular call can consist of one, the other, or both structures. An FM sweep is a broadband signal – that is, it contains a downward sweep through a range of frequencies. A CF tone is a narrowband signal: the sound stays constant at one frequency throughout its duration.
- Intensity: Echolocation calls have been measured at intensities anywhere between 60 and 140 decibels(Surlykee et al. 2008). Certain microbat species can modify their call intensity mid-call, lowering the intensity as they approach objects that reflect sound strongly. This prevents the returning echo from deafening the bat (Hiryu et al. 2007). Additionally, the so-called "whispering bats" have adapted low-amplitude echolocation so that their prey, moths, which are able to hear echolocation calls, are less able to detect and avoid an oncoming bat (Fullard 1997).
- Harmonic composition: Calls can be composed of one frequency, or multiple frequencies comprising a harmonic seriesHarmonic series (music)Pitched musical instruments are often based on an approximate harmonic oscillator such as a string or a column of air, which oscillates at numerous frequencies simultaneously. At these resonant frequencies, waves travel in both directions along the string or air column, reinforcing and canceling...
. In the latter case, the call is usually dominated by a certain harmonic ("dominant" frequencies are those present at higher intensities than other harmonics present in the call).
- Call duration: A single echolocation call (a call being a single continuous trace on a sound spectrogramSpectrogramA spectrogram is a time-varying spectral representation that shows how the spectral density of a signal varies with time. Also known as spectral waterfalls, sonograms, voiceprints, or voicegrams, spectrograms are used to identify phonetic sounds, to analyse the cries of animals; they were also...
, and a series of calls comprising a sequence or pass) can last anywhere from 0.2 to 100 milliseconds in duration, depending on the stage of prey-catching behavior that the bat is engaged in. For example, the duration of a call usually decreases when the bat is in the final stages of prey capture – this enables the bat to call more rapidly without overlap of call and echo. Reducing duration comes at the cost of having less total sound available for reflecting off objects and being heard by the bat.
- Pulse interval: The time interval between subsequent echolocation calls (or pulses) determines two aspects of a bat's perception. First, it establishes how quickly the bat's auditory scene information is updated. For example, bats increase the repetition rate of their calls (that is, decrease the pulse interval) as they home in on a target. This allows the bat to get new information regarding the target's location at a faster rate when it needs it most. Secondly, the pulse interval determines the maximum range that bats can detect objects. This is because bats can only keep track of the echoes from one call at a time; as soon as they make another call they stop listening for echoes from the previously made call (Wilson and Moss 2004). For example, a pulse interval of 100 ms (typical of a bat searching for insects) allows sound to travel in air roughly 34 meters so a bat can only detect objects as far away as 17 meters (the sound has to travel out and back). With a pulse interval of 5 ms (typical of a bat in the final moments of a capture attempt), the bat can only detect objects up to 85 cm away. Therefore the bat constantly has to make a choice between getting new information updated quickly and detecting objects far away.
FM Signal Advantages
The major advantage conferred by an FM signal is extremely precise range discrimination, or localization, of the target. J.A. Simmons demonstrated this effect with a series of elegant experiments that showed how bats using FM signals could distinguish between two separate targets even when the targets were less than half a millimeter apart. This amazing ability is due to the broadband sweep of the signal, which allows for better resolution of the time delay between the call and the returning echo, thereby improving the cross correlation of the two. Additionally, if harmonic frequencies are added to the FM signal, then this localization becomes even more precise. (Jones and Teeling 2006; Zupanc 2004; Simmons and Stein 1980; Grinnell 1995)One possible disadvantage of the FM signal is a decreased operational range of the call. Because the energy of the call is spread out among many frequencies, the distance at which the FM-bat can detect targets is limited (Fenton 1995). This is in part because any echo returning at a particular frequency can only be evaluated for a brief fraction of a millisecond, as the fast downward sweep of the call does not remain at any one frequency for long (Grinnell 1995).
CF signal advantages
The structure of a CF signal is adaptive in that it allows the CF-bat to detect both the velocity of a target, and the fluttering of a target's wings as Doppler shifted frequencies. A Doppler shift is an alteration in sound wave frequency, and is produced in two relevant situations: when the bat and its target are moving relative to each other, and when the target's wings are oscillating back and forth. CF-bats must compensate for Doppler shifts, lowering the frequency of their call in response to echoes of elevated frequency - this ensures that the returning echo remains at the frequency to which the ears of the bat are most finely tuned. The oscillation of a target's wings also produces amplitude shifts, which gives a CF-bat additional help in distinguishing a flying target from a stationary one. (Schnitzler and Flieger 1983; Zupanc 2004; Simmons and Stein 1980; Grinnell 1995; Neuweiler 2003; Jones and Teeling 2006)Additionally, because the signal energy of a CF call is concentrated into a narrow frequency band, the operational range of the call is much greater than that of an FM signal. This relies on the fact that echoes returning within the narrow frequency band can be summed over the entire length of the call, which maintains a constant frequency for up to 100 milliseconds (Grinnell 1995; Fenton 1995)
Acoustic environments of FM and CF signals
- FM: An FM component is excellent for hunting prey while flying in close, cluttered environments. Two aspects of the FM signal account for this fact: the precise target localization conferred by the broadband signal, and the short duration of the call. The first of these is essential because in a cluttered environment, the bats must be able to resolve their prey from large amounts of background noise. The 3D localization abilities of the broadband signal enable the bat to do exactly that, providing it with what Simmons and Stein (1980) call a "clutter rejection strategy." This strategy is further improved by the use of harmonics, which, as previously stated, enhance the localization properties of the call. The short duration of the FM call is also best in close, cluttered environments because it enables the bat to emit many calls extremely rapidly without overlap. This means that the bat can get an almost continuous stream of information – essential when objects are close, because they will pass by quickly – without confusing which echo corresponds to which call. (Neuweiler 2003; Simmons and Stein 1980; Jones and Teeling 2006; Fenton 1995)
- CF: A CF component is often used by bats hunting for prey while flying in open, clutter-free environments, or by bats that wait on perches for their prey to appear. The success of the former strategy is due to two aspects of the CF call, both of which confer excellent prey-detection abilities. First, the greater working range of the call allows bats to detect targets present at great distances – a common situation in open environments. Second, the length of the call is also suited for targets at great distances: in this case, there is a decreased chance that the long call will overlap with the returning echo. The latter strategy is made possible by the fact that the long, narrowband call allows the bat to detect Doppler shifts, which would be produced by an insect moving either towards or away from a perched bat. (Neuweiler 2003; Simmons and Stein 1980; Jones and Teeling 2006; Fenton 1995)
Neural mechanisms in the brain
Because bats use echolocation to orient themselves and to locate objects, their auditory systems are adapted for this purpose, highly specialized for sensing and interpreting the stereotyped echolocation calls characteristic of their own species. This specialization is evident from the inner ear up to the highest levels of information processing in the auditory cortex.Inner ear and primary sensory neurons
Both CF and FM bats have specialized inner ears which allow them to hear sounds in the ultrasonic range, far outside the range of human hearing. Although in most other aspects, the bat's auditory organs are similar to those of most other mammals, certain bats (horseshoe bats, Rhinolophus spp. and the moustached bat, Pteronotus parnelii) with a constant frequency (CF) component to their call (known as high duty cycle bats) do have a few additional adaptations for detecting the predominant frequency (and harmonics) of the CF vocalization. These include a narrow frequency "tuning" of the inner ear organs, with an especially large area responding to the frequency of the bat's returning echoes (Neuweiler 2003).The basilar membrane
Basilar membrane
The basilar membrane within the cochlea of the inner ear is a stiff structural element that separates two liquid-filled tubes that run along the coil of the cochlea, the scala media and the scala tympani .-Function:...
within the cochlea
Cochlea
The cochlea is the auditory portion of the inner ear. It is a spiral-shaped cavity in the bony labyrinth, making 2.5 turns around its axis, the modiolus....
contains the first of these specializations for echo information processing. In bats that use CF signals, the section of membrane that responds to the frequency of returning echoes is much larger than the region of response for any other frequency. For example, in Rhinolophus ferrumequinum, the horseshoe bat, there is a disproportionately lengthened and thickened section of the membrane that responds to sounds around 83 kHz, the constant frequency of the echo produced by the bat's call. This area of high sensitivity to a specific, narrow range of frequency is known as an "acoustic fovea
Fovea
The fovea centralis, also generally known as the fovea , is a part of the eye, located in the center of the macula region of the retina....
" (Schuller and Pollack 1979).
Odontocetes (toothed whales and dolphins) have similar cochlear specializations to those found in bats. Odontocetes also have the highest neural investment of any cochleae reported to date with ratios of greater than 1500 ganglion cells/mm of basilar membrane.
Further along the auditory pathway, the movement of the basilar membrane results in the stimulation of primary auditory neurons. Many of these neurons are specifically "tuned" (respond most strongly) to the narrow frequency range of returning echoes of CF calls. Because of the large size of the acoustic fovea, the number of neurons responding to this region, and thus to the echo frequency, is especially high (Carew 2001).
Inferior colliculus
In the Inferior colliculus
Inferior colliculus
The inferior colliculus is the principal midbrain nucleus of the auditory pathway and receives input from several more peripheral brainstem nuclei in the auditory pathway, as well as inputs from the auditory cortex...
, a structure in the bat's midbrain, information from lower in the auditory processing pathway is integrated and sent on to the auditory cortex. As George Pollak and others showed in a series of papers in 1977, the interneurons in this region have a very high level of sensitivity to time differences, since the time delay between a call and the returning echo tells the bat its distance from the target object. Especially interesting is that while most neurons respond more quickly to stronger stimuli, collicular neurons maintain their timing accuracy even as signal intensity changes.
These interneurons are specialized for time sensitivity in several ways. First, when activated, they generally respond with only one or two action potential
Action potential
In physiology, an action potential is a short-lasting event in which the electrical membrane potential of a cell rapidly rises and falls, following a consistent trajectory. Action potentials occur in several types of animal cells, called excitable cells, which include neurons, muscle cells, and...
s. This short duration of response allows their action potentials to give a very specific indication of the exact moment of the time when the stimulus arrived, and to respond accurately to stimuli that occur close in time to one another. In addition, the neurons have a very low threshold of activation – they respond quickly even to weak stimuli. Finally, for FM signals, each interneuron is tuned to a specific frequency within the sweep, as well as to that same frequency in the following echo. There is specialization for the CF component of the call at this level as well. The high proportion of neurons responding to the frequency of the acoustic fovea actually increases at this level (Carew 2001, Pollak 1977, Zupanc 2004).
Auditory cortex
The auditory cortex in bats is quite large in comparison with other mammals (Anderson 1995). Various characteristics of sound are processed by different regions of the cortex, each providing different information about the location or movement of a target object. Most of the existing studies on information processing in the auditory cortex of the bat have been done by Nobuo SugaNobuo Suga
Nobuo Suga is a Japanese biologist, famous for his research on the neurophysiology of hearing, and echolocation in bats.-Life:After achieving a bachelors degree in biology at Tokyo Metropolitan University in 1958, Nobuo studied for his doctoral thesis on the neurophysiology of hearing with Yatsuji...
on the mustached bat, Pteronotus parnellii. This bat's call has both CF tone and FM sweep components.
Suga and his colleagues have shown that the cortex contains a series of "maps" of auditory information, each of which is organized systematically based on characteristics of sound such as frequency
Frequency
Frequency is the number of occurrences of a repeating event per unit time. It is also referred to as temporal frequency.The period is the duration of one cycle in a repeating event, so the period is the reciprocal of the frequency...
and amplitude
Amplitude
Amplitude is the magnitude of change in the oscillating variable with each oscillation within an oscillating system. For example, sound waves in air are oscillations in atmospheric pressure and their amplitudes are proportional to the change in pressure during one oscillation...
. The neurons in these areas respond only to a specific combination of frequency and timing (sound-echo delay), and are known as combination-sensitive neurons.
The systematically organized maps in the auditory cortex respond to various aspects of the echo signal, such as its delay and its velocity. These regions are composed of "combination sensitive" neurons that require at least two specific stimuli to elicit a response. The neurons vary systematically across the maps, which are organized by acoustic features of the sound and can be two dimensional. The different features of the call and its echo are used by the bat to determine important characteristics of their prey. The maps include:
- FM-FM area: This region of the cortex contains FM-FM combination-sensitive neurons. These cells respond only to the combination of two FM sweeps: a call and its echo. The neurons in the FM-FM region are often referred to as "delay-tuned," since each responds to a specific time delay between the original call and the echo, in order to find the distance from the target object (the range). Each neuron also shows specificity for one harmonic in the original call and a different harmonic in the echo. The neurons within the FM-FM area of the cortex of Pteronotus are organized into columns, in which the delay time is constant vertically but increases across the horizontal plane. The result is that range is encoded by location on the cortex, and increases systematically across the FM-FM area (Suga et al. 1975, Suga et al. 1979, Neuweiler 2003, Carew 2001).
- CF-CF area: Another kind of combination-sensitive neuron is the CF-CF neuron. These respond best to the combination of a CF call containing two given frequencies – a call at 30 kHz (CF1) and one of its additional harmonics around 60 or 90 kHz (CF2 or CF3) – and the corresponding echoes. Thus, within the CF-CF region, the changes in echo frequency caused by the Doppler shift can be compared to the frequency of the original call to calculate the bat's velocity relative to its target object. As in the FM-FM area, information is encoded by its location within the map-like organization of the region. The CF-CF area is first split into the distinct CF1-CF2 and CF1-CF3 areas. Within each area, the CF1 frequency is organized on an axis, perpendicular to the CF2 or CF3 frequency axis. In the resulting grid, each neuron codes for a certain combination of frequencies that is indicative of a specific velocity (Suga et al. 1975, Suga et al. 1987, Carew 2001).
- DSCF area: This large section of the cortex is a map of the acoustic fovea, organized by frequency and by amplitude. Neurons in this region respond to CF signals that have been Doppler shifted (in other words, echoes only) and are within the same narrow frequency range to which the acoustic fovea responds. For Pteronotus, this is around 61 kHz. This area is organized into columns, which are arranged radially based on frequency. Within a column, each neuron responds to a specific combination of frequency and amplitude. Suga's studies have indicated that this brain region is necessary for frequency discrimination (Suga et al. 1975, Suga et al. 1987, Carew 2001).
Toothed whales
Dolphin
Dolphins are marine mammals that are closely related to whales and porpoises. There are almost forty species of dolphin in 17 genera. They vary in size from and , up to and . They are found worldwide, mostly in the shallower seas of the continental shelves, and are carnivores, mostly eating...
s, porpoise
Porpoise
Porpoises are small cetaceans of the family Phocoenidae; they are related to whales and dolphins. They are distinct from dolphins, although the word "porpoise" has been used to refer to any small dolphin, especially by sailors and fishermen...
s, river dolphin
River dolphin
River dolphins are the four living species of dolphin that reside in freshwater rivers and estuaries. River dolphins inhabit areas of Asia and South America. They are classed in the Platanistoidea superfamily of cetaceans. Three species live in fresh water rivers. The fourth species, the La Plata...
s, killer whales and sperm whale
Sperm Whale
The sperm whale, Physeter macrocephalus, is a marine mammal species, order Cetacea, a toothed whale having the largest brain of any animal. The name comes from the milky-white waxy substance, spermaceti, found in the animal's head. The sperm whale is the only living member of genus Physeter...
s, because they live in an underwater habitat that has favourable acoustic characteristics and where vision
Visual perception
Visual perception is the ability to interpret information and surroundings from the effects of visible light reaching the eye. The resulting perception is also known as eyesight, sight, or vision...
is extremely limited in range due to absorption
Underwater
Underwater is a term describing the realm below the surface of water where the water exists in a natural feature such as an ocean, sea, lake, pond, or river. Three quarters of the planet Earth is covered by water...
or turbidity
Turbidity
Turbidity is the cloudiness or haziness of a fluid caused by individual particles that are generally invisible to the naked eye, similar to smoke in air. The measurement of turbidity is a key test of water quality....
.
Cetacean evolution consisted of three main radiations. Throughout the middle and late Eocene periods (49-31.5 million years ago), archaeocetes, primitive toothed Cetacea that arose from terrestrial mammals with the creation of aquatic adaptations, were the only known archaic Cetacea. These primitive aquatic mammals did not posses the ability to echolocate, although they did have slightly adapted underwater hearing. The morphology of acoustically isolated ear bones in basilosaurid archaeocetes indicates that this order had directional hearing underwater at low to mid frequencies by the late middle Eocene. However, with the extinction of archaeocete at the onset of the Oligocene, two new lineages in the early Oligocene period (31.5-28 million years ago) compromised a second radiation. These early mysticete (baleen whales) and odontocete can be dated back to the middle Oligocene in New Zealand. Based on past phylogenies, it has been found that the evolution of odontocetes is monophyletic, suggesting that echolocation evolved only once 36 to 34 million years ago. Dispersal rates routes of early odontocetes included transoceanic travel to new adaptive zones. The third radiation occurred later in the Neogene, when present dolphins and their relatives evolved to be the most common species in the modern sea.
The evolution of echolocation could be attributed several theories. There are two proposed drives for the hypotheses of cetacean radiation, one biotic and the other abiotic in nature. The first, adaptive radiation, is the result of a rapid divergence into new adaptive zones. This results in diverse, ecologically different clades that are incomparable. Clade Neocete (crown cetacean) has been characterized by an evolution from archaeocetes and a dispersion across the world’s oceans, and even estuarites and rivers. These ecological opportunities were the result of abundant dietary resources with low competition for hunting. This hypothesis of lineage diversification, however, can be unconvincing due to a lack of support for rapid speciation early in cetacean history. A second, more abiotic drive is more supported. Physical restructuring of the oceans has played a role in echolocation radiation. This was a result of global climate change at the Eocene-Oligocene boundary; from a greenhouse to an icehouse world. Tectonic openings created the emergence of the Southern ocean with a free flowing Antarctic Circumpolar current (Fordyce 1980, 2003; Lindberg & Pyenson 2007; Steeman et al. 2009). These events allowed for a selection regime characterized by the ability to locate and capture prey in turbid river waters, or allow odontocetes to invade and feed at depths below the photic zone. Further studies have found that echolocation below the photic zone could have been a predation adaptation to diel migrating
Diel vertical migration
Diel vertical migration, also known as diurnal vertical migration, is a pattern of movement that some organisms living in the ocean and in lakes undertake each day. Usually organisms move up to the epipelagic zone at night and return to the mesopelagic zone of the oceans or to the hypolimnion zone...
cephalopods. Since its advent, there has been adaptive radiation
Adaptive radiation
In evolutionary biology, adaptive radiation is the evolution of ecological and phenotypic diversity within a rapidly multiplying lineage. Starting with a recent single ancestor, this process results in the speciation and phenotypic adaptation of an array of species exhibiting different...
especially in the Delphinidae family (dolphins) in which echolocation has become extremely derived.
One specific type of echolocation, narrow-band high frequency (NBHF) clicks, evolved at least four times in groups of odontocetes, including pygmy sperm whale (Kogiidae) and porpoise (Phocoenidae) families, Pontoporia blainvillei
La Plata Dolphin
The La Plata Dolphin or Franciscana is found in coastal Atlantic waters of southeastern South America. Taxonomically it is a member of the river dolphin group and the only one that actually lives in the ocean and saltwater estuaries, rather than inhabiting exclusively freshwater...
, the genus Cephalorhynchus
Cephalorhynchus
Cephalorhynchus is a genus in the dolphin family Delphinidae. It consists of four species:*Commerson's Dolphin, Cephalorhyncus commersonii*Chilean Dolphin, Cephalorhyncus eutropia*Heaviside's Dolphin, Cephalorhyncus heavisidii...
, and part of the genus Lagenorhynchus
Lagenorhynchus
Lagenorhynchus is a genus in the order Cetacea, traditionally containing six species:* white-beaked dolphin, Lagenorhynchus albirostris* Atlantic white-sided dolphin, Lagenorhynchus acutus...
. These high frequency clicks likely evolved as adaptation of predator avoidance, as they inhabit areas that have many killer whales and the signals are inaudible to killer whales due to the absence of energy below 100 kHz. Another reason for variation in echolocation frequencies is habitat. Shallow waters, where many of these species live, tend to have more debris; a more directional transmission reduces clutter in reception.
Toothed whales emit a focused beam of high-frequency clicks in the direction that their head is pointing. Sounds are generated by passing air from the bony nares through the phonic lips. These sounds are reflected by the dense concave bone of the cranium and an air sac at its base. The focused beam is modulated by a large fatty organ known as the 'melon'. This acts like an acoustic lens because it is composed of lipids of differing densities. Most toothed whales use clicks in a series, or click train, for echolocation, while the sperm whale may produce clicks individually. Toothed whale whistles do not appear to be used in echolocation. Different rates of click production in a click train give rise to the familiar barks, squeals and growls of the bottlenose dolphin
Bottlenose Dolphin
Bottlenose dolphins, the genus Tursiops, are the most common and well-known members of the family Delphinidae, the family of oceanic dolphins. Recent molecular studies show the genus contains two species, the common bottlenose dolphin and the Indo-Pacific bottlenose dolphin , instead of one...
. A click train with a repetition rate over 600 per second is called a burst pulse. In bottlenose dolphins, the auditory brain response resolves individual clicks up to 600 per second, but yields a graded response for higher repetition rates.
It has been suggested that some smaller toothed whales may have their tooth arrangement suited to aid in echolocation. The placement of teeth in the jaw of a bottlenose dolphin, as an example, are not symmetrical when seen from a vertical plane, and this asymmetry could possibly be an aid in the dolphin sensing if echoes from its biosonar are coming from one side or the other. However, this idea lacks experimental support.
Echoes are received using complex fatty structures around the lower jaw as the primary reception path, from where they are transmitted to the middle ear via a continuous fat body (Ketten 1992,2000). Lateral sound may be received though fatty lobes surrounding the ears with a similar density to water. Some researchers believe that when they approach the object of interest, they protect themselves against the louder echo by quietening the emitted sound. In bats this is known to happen, but here the hearing sensitivity is also reduced close to a target.
Before the echolocation abilities of "porpoises" were officially discovered, Jacques Yves Cousteau suggested that they might exist. In his first book, The Silent World
The Silent World: A Story of Undersea Discovery and Adventure
The Silent World is a 1953 book co-authored by Captain Jacques-Yves Cousteau and Frédéric Dumas and edited by James Dugan. Although a French national, Cousteau wrote the book in English...
(1953, pp. 206–207), he reported that his research vessel, the Élie Monier, was heading to the Straits of Gibraltar and noticed a group of porpoises following them. Cousteau changed course a few degrees off the optimal course to the center of the strait, and the porpoises followed for a few minutes, then diverged toward mid-channel again. It was obvious that they knew where the optimal course lay, even if the humans didn't. Cousteau concluded that the cetaceans had something like sonar
Sonar
Sonar is a technique that uses sound propagation to navigate, communicate with or detect other vessels...
, which was a relatively new feature on submarines.
Oilbirds and swiftlets
OilbirdOilbird
The Oilbird , also known as Guácharo, is a bird found in the northern areas of South America . They are nocturnal feeders on the fruits of the Oil Palm and tropical laurels, and are the only nocturnal fruit eating birds in the world...
s and some species of swiftlet
Swiftlet
Swiftlets are birds contained within the four genera Aerodramus, Hydrochous, Schoutedenapus and Collocalia. They form the Collocaliini tribe within the swift family Apodidae. The group contains around thirty species mostly confined to southern Asia, south Pacific islands, and northeastern...
are known to use a relatively crude form of echolocation compared to that of bats and dolphins. These nocturnal birds emit calls while flying and use the calls to navigate through trees and caves where they live.
Shrews and tenrecs
Terrestrial mammals other than bats known to echolocate include two genera (SorexSorex
The genus Sorex includes many of the common shrews of Eurasia and North America. Members of this genus, known as long-tailed shrews, are the only members of the tribe Soricini of the subfamily Soricinae...
and Blarina) of shrews and the tenrecs of Madagascar
Madagascar
The Republic of Madagascar is an island country located in the Indian Ocean off the southeastern coast of Africa...
. These include the wandering shrew (Sorex vagrans), the common or Eurasian shrew (Sorex araneus), and the short-tailed shrew (Blarina brevicauda). The nature of shrew sounds unlike those of bats are low amplitude, broadband, multi-harmonic and frequency modulated. They contain no ‘echolocation clicks’ with reverberations and would seem to be used for simple, close range spatial orientation. In contrast to bats, shrews use echolocation only to investigate their habitat rather than additionally to pinpoint food.
External links
- The British Library Sound Archive 150,000 recordings of over 10,000 species, including many echolocation recordings
- International Bioacoustics Council links to many bioacoustics resources
- Listen to Nature has bat and swiftlet sonar signals
- Bat Ecology & Bioacoustics Lab
- Keep your ears peeled article on physics.org
- Batlab at Brown Univiersity JA Simmons Lab Website