Given the extraordinary powers of echolocation in bats, it is not surprising that this group has received the most attention. However, they are not the only mammals to have evolved echolocation. Who invented sonar millions of years before the Navy?

Echolocation, the ability to bounce sound off surrounding objects and register the returning echoes, has evolved multiple times in animals. Given the extraordinary powers of echolocation in bats, it is not surprising that this group has received the most attention. Toothed whales, however, are also capable of sophisticated echolocation, and more rudimentary systems are found in a number of small, ground-dwelling mammals (as well as in at least two groups of birds, swiftlets and oilbirds).

Whilst bats and echolocation are almost synonymous, the convergence in the whales suggest that this sensory modality is a predictable outcome when facing certain challenges. In addition, echolocation has evolved in some small mammals and bats are descended from a shrew-like creature, which has led to the suggestion that bats were already able to echolocate when they took to the skies. However, in flying bats, sound emission is synchronised with exhalation and wing beat, so reducing the energetic costs of echolocation in flight to almost zero, while its benefits in an open aerial environment are huge. For terrestrial mammals, the energetic cost of generating high-intensity ultrasonic calls is substantial and the benefit of echolocation presumably rather low, because they live in complex, cluttered environments, where strong signal reflection would make echo processing very difficult (although one should note that bats navigating amongst trees and branches have overcome this problem with astonishing success). In water, sound travels almost five times faster than in air, favouring acoustics over vision (that is generally limited underwater).

Toothed whales

Vocalisations in general are of vast importance to toothed whales (Odontoceti), a diverse, widely distributed cetacean suborder with more than 70 species that includes dolphins, porpoises, beaked whales, sperm whales (Physeter macrocephalus) and orcas (Orcinus orca). Many species produce a variety of calls to communicate, such as the frequency-modulated whistles of dolphins, and all toothed whales are probably capable of echolocation. Ultrasonic hearing was first demonstrated in dolphins in the 1950s, and experiments with blindfolded animals swimming through obstacle courses later confirmed the use of echolocation for orientation. It is also employed for the detection and localisation of prey and the general differentiation of surrounding objects. The acoustic world of echolocating cetaceans is probably very different from that of bats, because water has greater impedance due to its higher density. While most objects in a bat’s environment should produce echoes, structures such as the swim bladder or skeleton of fish are likely to stand out underwater, enabling dolphins to find even prey that is buried in sediment.

Signal production and reception

The echolocation mechanism of toothed whales differs markedly from that of insectivorous bats, which produce tonal calls in their larynx, emit them through their mouth or nose and receive them with their large ears. Toothed whales generate click-like vocalisations using phonic lips (“monkey lips”) and associated air sacs in their nasal passages (interestingly, clicks are also produced by fruit bats in the genus Rousettus, but they use their tongue). The clicks are transmitted through a waxy “melon” that is located on the forehead and contains lipids of different densities. It acts as an acoustic lens and emits a focussed beam of sound. The echoes are primarily received through the lower jaw, which is surrounded by complex fatty structures, and conveyed to the ear through a continuous fat-filled canal. It has been suggested that modified tooth arrangements in some species may aid echolocation, for example in bottlenose dolphins (Tursiops truncates), where an asymmetrical placement of teeth could provide directional information. Evidence suggests that the phonic lips and associated acoustic fat bodies have evolved once in odontocetes, but have been subsequently modified in relation to click structure.

Despite these differences between dolphins and bats, their cochleae show anatomical convergence with respect to several features, such as the outer hair cells, which are shorter and stiffer compared to other mammals. Furthermore, a recent study has found evidence for molecular convergence related to echolocation. It revealed multiple parallel amino acid changes in the motor protein Prestin, which seems to be responsible for high-frequency sensitivity and selectivity in the auditory system of mammals. This sequence convergence is probably due to natural selection acting similarly on these two groups of echolocating mammals.

Probably associated with the cognitive demands of echolocation is the large size of cetacean brains (when measured relative to body size, only human brains are larger). In dolphins, most auditory nuclei in the brain stem are particularly well developed and the cerebellum is disproportionately large. Echolocation shows great finesse in odontocetes and bottlenose dolphins can resolve up to 600 individual echolocation clicks per second. There is evidence that the sensory input from echolocation can be combined with vision (a process known as cross-modal recognition), echoing of course similar capacities for signal combination, such as information from the eyes and infrared-sensitive pits in crotaline snakes.

Signal structure

Most toothed whale clicks are ultrasonic, although sperm whales mainly use lower frequencies that are audible to humans. Interestingly, some fish (e.g. cod and shad) have evolved sensitivity to ultrasound to escape from echolocating cetaceans, analogous to the response of some insects that are preyed upon by bats. Odontocete clicks, which often occur in series called click trains, are usually much shorter than bat calls (possibly to ensure sufficient temporal resolution) and less diverse in their structure. There are basically two different types – short, high-intensity broadband signals (e.g. in bottlenose dolphins) and longer, more narrowband signals with lower intensity. The latter have evolved independently in a number of phylogenetically distant groups, namely the porpoises (Phocoenidae), the dolphin genus Cephalorhynchus, the pygmy sperm whale (Kogia breviceps) and apparently the La Plata dolphin (Pontoporia blainvillei), all of which have also lost their ability to produce the communicative whistles. Their clicks have peak frequencies above 100 kHz, which seems to be outside the hearing range of predatory orcas. It has been hypothesised that these species might be particularly vulnerable to predation from orcas and could have evolved high-pitched clicks as a predator-avoidance mechanism. Such “acoustic crypsis” has been demonstrated in various other taxa, including insects, frogs and birds.

Ground-dwelling mammals

Not only bats and whales, but so too a number of small, terrestrial mammals have evolved limited echolocative capacities, such as shrews (Soricidae) and tenrecs (Tenrecidae). Not much is known about echolocation in these animals and it may be difficult to distinguish between pulses employed for echolocation and those used in communication. Most studied are the shrews, where experimental studies in several species suggested that they produce ultrasonic squeaks to explore their environment. For example, common shrews (Sorex araneus) and white-toothed shrews (Crocidura russula) generate high-pitched (although not necessarily ultrasonic), broadband “twittering” calls in their larynx, and behavioural tests indicated that they are used for echo-based orientation rather than communication. However, these calls are faint, thus operating only at close range, and generally much less sophisticated than the laryngeal calls of bats, thus probably providing only limited information. They probably aid simple, close-range spatial orientation, such as the identification of a route through the habitat or probing of the habitat type, and might also help the shrews to find protective cover from predators. It is, however, considered relatively unlikely that the echo information is used for foraging.

The Madagascan tenrecs are particularly known for their intriguing convergences with hedgehogs, but at least some species seem to possess echolocative capacities. One study provided evidence that tenrecs use short low-frequency tongue clicks for orientation. Several rodents produce ultrasound, the main purpose of which seems to be communication, particularly between mother and offspring (although some studies indicated echolocative abilities in rats). Interestingly, there are also reports on human “echolocation”, where blind people use the echoes of actively created sounds to navigate their environment.