What on earth could an elephant or treehoppers have in common with a seismometer?

Vibrations are seldom important in the lives of humans – we mainly rely on vision and hearing and can detect vibrations merely with sensitive equipment. Numerous animals, however, cannot only sense them but also use them to communicate with each other, exchanging low-frequency signals that propagate through a substrate, such as soil or plant stems. In fact, there is a whole vibrational world out there that we have only just begun to appreciate. Vibrational communication seems to be an ancient sensory mode and is not only much more important and widespread than previously thought, but has evolved multiple times in diverse animal groups. Initially, the seismic channel was assumed to be a quiet one, but it is now appreciated that many animals, particularly the insects, signal in a complex vibrational environment that might be cluttered with noise (e.g. from wind or rain) and, even worse, inhabited by eavesdropping enemies.

Different mechanisms are used for producing vibrations, such as drumming, tremulation (body vibration) or stridulation (rubbing together body parts). The resulting signals are often species-specific and sometimes even individually distinct, and information is encoded in frequency or temporal patterns. Signal detection occurs by a somatosensory mechanism, where vibration-sensitive mechanoreceptors can project directly to the brain, or via bone conduction to the inner ear, or indeed both. The functions of vibrational signals are manifold. Within species, they can be used to identify or localise potential mates, during courtship (particularly in arthropods), in competitive interactions, or to signal alarm. Many social insects employ vibrations to coordinate the actions of group members, for example in cooperative foraging. Substrate-borne signals also play a role in interspecific communication, usually between predator and prey. Not only can they detect each other by means of the vibrations they generate, but predators might mimic prey signals to actively attract a meal, while prey might use vibrations to warn or challenge an enemy.

Vibrational communication has a number of advantages. Seismic waves attenuate less rapidly than air-borne sound waves and can travel over considerable distance (believed to be up to 16 km in elephants). Transmission range and velocity, however, depend on the properties of the substrate as well as on the signal energy, which for percussive signals is related to the size and muscular power of the producer. Therefore, in small animals vibrational signals are rather short-ranging. But as the relationship between signaller size and signal frequency that constrains air-borne sound transmission is relaxed in seismic transmission, even small animals can efficiently produce low-frequency substrate-borne signals. Compared to visual communication that needs both light and line of sight, vibrational communication is less limited and thus in certain conditions more effective. However, as a consequence of the long wavelength of seismic signals, the emitter can be hard to locate, and vibrations are often produced incidentally (e.g. through feeding or locomotion). It is important to note that vibrations and other information channels need not be mutually exclusive, but can be used in combination (multimodal signalling).

Vertebrates

Mammals

Vibrational signalling in mammals is best known in the form of footdrumming, a behaviour that has evolved independently in several groups. It is particularly well developed in the solitary, nocturnal kangaroo rats in the genus Dipodomys. Banner-tailed kangaroo rats (D. spectabilis) footdrum during courtship, to signal territory ownership and even when encountering a snake. Here, the drumming probably conveys that the rat is too alert for a successful ambush, thus preventing the snake’s pursuit. Unsurprisingly, seismic communication plays a major role in the life of subterranean mammals that are adapted to a life underground, such as blind mole rats. Ehrenberg’s mole rat (Spalax ehrenbergi) produces substrate-borne signals by head thumping and might even use the reflections to detect underground obstacles in a form of “seismic echolocation”. There is growing evidence that also the highly social elephants employ seismic signals (generated by low-frequency vocalisations coupling with the ground or by percussion) for long-distance communication with conspecifics. Most likely the feet are involved in signal reception, as elephants adopt particular postures in response to seismic stimuli. The dermis of fore and hind feet contains clusters of Pacinian corpuscles, and the large fatty cushions might play a role in impedance matching at the air-ground interface.

Birds

At least some birds are sensitive to seismic signals and they employ Herbst corpuscles, which are convergent with the Pacinian corpuscles of mammals. Shorebirds, kiwis and ibises detect prey-generated vibrations with the help of a sensitive bill-tip organ, but birds also produce vibrations themselves, which might betray their approach to prey (e.g. wolf spiders Schizocosa ocreata perceive bird calls as vibrations transmitted through the substrate). Pigeons (Columba livia) have Herbst corpuscles in their legs, which might serve as a kind of warning device, possibly in the context of predator avoidance. It has also been reported that birds behave unusually before earthquakes.

Frogs

Due to their structurally unique sacculus (an otolithic organ in the inner ear) and opercularis system (a series of muscular and bony elements connecting the pectoral girdle with the inner ear), frogs possess the highest seismic sensitivity of all terrestrial vertebrates studied so far. Seismic communication in this group, however, has not been investigated extensively. The best-known example is the Puerto Rican white-lipped frog (Leptodactylus albilabris), where males call to females and simultaneously produce a seismic signal by thumping their gular pouch on the ground. It has been shown that the calls are used to attract females, while the vibrations help males to space themselves in a group of calling consexuals. Females of the common tree frog (Polypedates leucomystax) attract males at night by rhythmically tapping their rear toes on the substrate. In red-eyed tree frogs (Agalychnis callidryas), tadpoles escape arboreal predators by hatching early from egg clumps deposited on leaves overhanging pools of water. They use a complex strategy that is based on duration, interval and frequency of vibrational cues to identify predators and react appropriately. When threatened by a snake, all embryos in the clutch hatch rapidly, whereas a wasp attack prompts premature hatching of only the tadpole being grasped and its neighbours. However, rainstorms excite vibrations in clutches that are very similar to those of predators and false alarms are costly. Remarkably, these frogs use two characteristics of rainstorm vibrations not present in predator-generated vibrations to avoid premature hatching in response to rain.

Snakes

Contrary to common belief, snakes are able to perceive and react to substrate-borne as well as air-borne vibrations (despite lacking an outer ear and a tympanum). They can pick them up through their lower jaw, which typically rests on the ground and is connected with the inner ear, or detect them directly with receptors on their body surface. Substrate-borne signals seem to play a role in predator avoidance and prey capture in at least some species. Experiments with semi-fossorial horned desert vipers (Cerastes cerastes) showed that these ambush predators strongly rely on vibrational stimuli for capturing prey, the localisation of which is probably aided by the two halves of the lower jaw being independent. However, intraspecific seismic communication is considered unlikely (though not impossible) in snakes, mainly because there seems to be a frequency imbalance between sound production and vibrational sensitivity.

Invertebrates

Insects

Vibrational communication is amazingly widespread (and convergent) in insects. It is, in fact, the dominant mode of mechanical signalling, and this is probably related to the small body size of insects. Vibrations are produced by specific movements of the body or body parts. They are then received with vibration sensors located in the legs and put to multiple uses. They play a major role in mating (e.g. in the southern green stink bug Nezara viridula, where male and female engage in vibrational duets), but are also related to alarm (e.g. in termites that drum in response to predators and pathogenic fungi) and defensive behaviour (e.g. in Semiothisa aemulataria caterpillars that lower themselves to safety by a silk thread in response to vibrations produced by an approaching predator). Vibrations can furthermore coordinate interactions between members of social groups, as illustrated by a treehopper (Calloconophora pinguis) that has evolved a highly sophisticated vibrational signalling system to deal with the challenge of cooperative feeding on an ephemeral food source. Interspecific relationships might also rely on vibrations, such as in Thisbe irenea caterpillars, which use vibrations to attract ants that provide protection from predators, or in the case of “vibrational eavesdropping” by spiders.

Spiders

Spiders not only use vibrations to localise struggling insects in their webs, but are in fact masters of vibrational communication with highly sensitive vibration receptors in their cuticle. Male jumping spiders (Salticidae) produce a complex repertoire of multi-component seismic signals during courtship that were shown to strongly affect their mating success. The araneophagic jumping spiders in the genus Portia use vibrations to capture other spiders. Some invade their victim’s web and imitate the vibrational signals of caught insects, while Portia fimbriata mimics the vibrational signals of males of other spider species to attract and then prey on the females

Crustaceans

Some crustaceans also engage in vibrational communication. These include the fiddler crabs (genus Uca), highly successful burrowers in the mudflats of the tropics. They are famous for their courtship display, during which males wave their enlarged claw to attract females. However, in some species such as sand fiddler crabs (Uca pugilator), males also use the claw to drum on the ground, thus producing surface waves that might facilitate their localisation (particularly at night).

Annelids

Many annelid worms respond to substrate-borne vibrations produced by predators, such as earthworms that emerge from the soil to escape from digging moles. Humans have long made use of this by (unknowingly) imitating these vibrations to “harvest” worms as bait for fishing, using a technique known as worm charming. It has become a competitive sport, and there are even annual ‘World Worm Charming Championships’ held in Cheshire! But also other animals convergently exploit the worms’ anti-predator response, sending vibrations through the ground and preying on the surfacing individuals. These include several birds (e.g. lapwings and herring gulls), but, interestingly, also the North American wood turtle (Glyptemys insculpta), which stomps its front feet on the ground.