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Cocroft R.B. (2010) Vibrational Communication. In: Breed M.D. and Moore J., (eds.) Encyclopedia of Animal Behavior, volume 3, pp. 498-505 Oxford: Academic Press.

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Vibrational Communication R. B. Cocroft, University of Missouri, Columbia, MO, USA

Introduction The use of substrate vibrations for communication is widespread in arthropods, including insects, crabs, and Using Substrate Vibrations to Communicate spiders and other arachnids. It is estimated that 265 000 Of all forms of communication that make use of mechan- species of insects communicate with substrate vibration. ical vibrations propagating through a medium, vibrational However, the true number is probably much larger, communication is by far the most common. However, because this estimate includes only the species that have it is also the least familiar to biologists, and the least been formally named. For many groups of insects, there studied. One consequence of this lack of attention is that are far more species yet to be described; for example, in many of our inferences about this communication modal- addition to the 20 000 described species of leafhoppers, ity are based on a relatively small number of studies. there are an estimated 80 000 additional undescribed spe- Another is that many opportunities remain for ground- cies, mostly in tropical forests. Whatever the real num- breaking study of a complex and fascinating mode of bers, it is probably safe to say that 98% of the diversity of communication that occurs in taxa ranging from spiders insect vibrational signals remains unrecorded. A similar to elephants. situation likely exists in the other arthropod groups. How does the use of vibrations differ from that of In insects, vibrational communication represents an airborne sound? The two modalities are closely related. ancient communication modality, evolving before the ori- However, while organisms using sound are embedded gin of airborne sound communication. The cicadas and within the medium they use for communication, those their relatives provide a good illustration: vibrational com- using vibration are at the boundary between air and a munication is widespread, while airborne sound occurs denser medium such as soil, water, or a solid structure like only in the cicadas, where it is clearly derived with respect a plant stem. Communication takes place among organ- to vibrational communication (Figure 1). Even within the isms in contact with this dense medium, using vibrations cicadas, vibrational communication occurs in basal spe- that travel along its surface. Sound in air or water propa- cies, and it is possible that it occurs in many others, used in gates as a longitudinal pressure wave, with motion of the combination with airborne sound. Recent discovery of medium occurring in the direction of travel of the wave. vibrational signaling in a Gondwanan relict species,

In contrast, substrate vibrations propagate as a variety of along with comparative phylogenetic analysis, suggests wave types, with receivers generally detecting the com- that vibrational signaling may have evolved in the ances- ponent of medium motion perpendicular to the direction tors of today’s Hemiptera, some 230 million years ago. of travel of the wave. This difference in the nature of Vibrational communication is also widespread in ver- signal propagation leads to differences in the structures tebrates; again, the species known to communicate using used to produce and detect sound and vibration, and in this modality represent only the tip of the iceberg. There the properties of the signals themselves. is increasing evidence for its importance in frogs and some reptiles, including the veiled chameleon (Figure 2). Vibrational communication is widespread in mammals, Taxonomic Distribution particularly in rodents, and more recently documented

Terrestrial animal species generally spend much or all of in large species, including elephants. their time in contact with a substrate. Vibrations introduced into that substrate by the movement of other organisms provide a rich source of information about the Perception and Production of behavior and proximity of conspecifics, predators, or Vibrational Signals prey. Many species, from worms to spiders to elephants, have evolved means of detecting these vibrations, and the The substrates used for vibrational communication vary detection of substrate vibrations underlies many social and with taxonomic group and, to some extent, with size. In ecological interactions. A recurring theme in the study of addition, the nature of the substrate influences how signals vibrational communication is the discovery of taxa in propagate and how they are perceived. Vibrationally signal- which individuals not only passively monitor substrate ing mammals typically use the ground as a communication vibrations but also introduce vibrations into the substrate channel (vibrations of the earth’s surface are referred to as in order to influence the behavior of other individuals. seismic signals). In most cases, signals are produced by

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Vibrational Communication 499

Delphacidae

Cixiidae

Dictyopharidae

Cicadellidae

Membracidae

Substrate vibration Aetalionidae

Cicadidae

Tettigarctidae

Cercopidae

Aphrophoridae

Airborne sound

Substrate vibration

Airborne sound

Figure 1 Phylogeny of the Cicadomorpha, showing the distribution of signaling modality among families. Communication by airborne sound in cicadas is a derived state with respect to substrate vibration (phylogeny drawn from Cryan JR (2005) Molecular phylogeny of Cicadomorpha (Insecta: Hemiptera: Cicadoidea, Cercopoidea, and Membracoidea): Adding evidence to the controversy. Systematic Entomology 30: 563–574).

drumming with the feet or, for some subterranean species, tapping the head against the soil. In elephants, foot stomping and low-frequency vocal rumbles generate

ground-borne waves that travel long distances. Seismic communication also occurs in crabs, scorpions, and some insects and spiders. However, most insects, many spiders, most cases in frogs, and one lizard (Figure 2)useliving

plants as a communication channel. Plant tissues such as stems and leaves are excellent substrates through which to transmit signals because they have evolved to flex in

response to mechanical disturbances such as wind, and as a consequence, will transmit even extremely low-amplitude signals for a meter or more along stems. Almost any move-

ment on the surface of a plant will generate a mechanical disturbance, and as a result, species that communicate through plants have a variety of ways of producing signals. These include striking the substrate with feet, head, abdo-

men, or other body part, using direct muscle contractions to vibrate some part of the body (resulting in signals contain- ing harmonic series or relatively pure tones; see video

example 1, which shows the abdomen of a signaling male treehopper, Umbonia crassicornis), and/or using a frequency multiplier such as a stridulatory file and scraper. For non

percussive forms of signal production, vibrations produced through direct muscle contraction or specialized vibrating structures are transmitted through the legs into the substrate. Many spiders transmit signals through webs, and

Figure 2 A male veiled chameleon (Chameleo calyptratus). some insects produce signals on the water surface; this This species communicates using visual signals and plant-borne article, however, deals only with vibrations traveling through vibrational signals. solid substrates. Because living plants are such a widespread

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500 Vibrational Communication substrate, with much of the literature on the function and organs are also important in vibration sensing in insects, evolution of vibrational communication focused on this and possibly other sensory organs at the joints, the main channel, the following discussion draws largely from research function of which is likely proprioception. Spiders and on plant-dwelling insects and spiders. other arachnids have lyriform organs in the cuticle, composed A bare description of the means of signal production of parallel rows of slit sensillae, situated near the joints of gives little impression of the tremendous diversity and the legs and in other locations on the body and sensitive to esthetic appeal of vibrational signals, which can be lis- mechanical deformations of the cuticle. In both insects and tened to through a loudspeaker. Strictly percussive signals spiders, the presence of receptors in multiple legs in contact would seem to have limited possibilities for diversity, but with the substrate is important for the localization of the drumming signals of stoneflies, spiders, or kangaroo vibrational signals; at least for species the legs of which mice can be surprisingly intricate and diverse in rhythm span several centimeters, arrival time differences at differ- and timing. The more tonal signals produced by many ent legs provide directional cues. insects, such as leafhoppers or stink bugs, usually contain In frogs, the inner ear contains sensory organs that are frequency sweeps and often combine different elements in highly sensitive to substrate vibration. Vibration sensitiv- surprising and evocative ways. Small animals have diffi- ity is also widespread in other amphibians and in reptiles, culty producing airborne sounds because pressure gradi- involving vibration-sensitive structures in the ear as well ents are difficult to maintain over very short distances. In as peripheral sense organs in the body. Placental mammals particular, an acoustical ‘short circuit’ prevents small ani- have vibration-sensitive Pacinian corpuscles in the skin mals from effectively broadcasting low-frequency air- and some species have vibration-sensitive inner ear struc- borne. However, the problem does not exist for substrate tures. Recent work on elephants suggests that they may be vibrations and, as a result, small insects can produce receiving ground-borne vibrations through their feet and signals using frequencies typical of much larger species trunk, which transmit them to vibration-sensitive struc- that use airborne sound (Figure 3; signal example 1). The tures in the inner ear. result is a hidden but rich and sometimes enchanting vibrational ‘soundscape’ contained within the surfaces around us in natural environments. The Ecological Context of Vibrational For most animals using substrate vibrations to commu- Communication nicate, the legs are the body part in contact with the sub- The Vibrational Environment strate, and the legs either contain the vibration sensors, or in vertebrates, serve as transmission channels to vibration- There is a pervasive misconception in the animal commu- sensitive structures in the ear. Insects perceive substrate- nication literature that vibrational communication occurs borne vibrations using an array of sensory receptors in in a ‘private channel’. This view probably stems from our their legs. The most sensitive are the subgenual organs, own insensitivity to substrate-borne vibration and our located in the fluid-filled cavity within each tibia and corresponding need for technology to gain access to the sensitive to movements of the tibia, especially along the world of vibrational interactions. However, most animal long axis of the tibia. In cockroaches, the subgenual organ species are not similarly handicapped. In nature, individuals is also sensitive to airborne sound. The femoral chordotonal that produce and respond to vibrational signals do so in an

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Frequency (kHz) 100

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Time (s) Figure 3 Vibrational signals of the stinkbug Edessa rufomarginata, recorded at Palo Verde, Costa Rica. The signaler was just over 1 cm long (shown in photo inset), but its signal frequency is as low as that of much larger species that use airborne sound.

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Vibrational Communication 501 environment rich with predators exquisitely equipped to Substrate Properties and Signal Evolution detect and localize vibrational signals. Recent work shows The vibrational signals of arthropods and rodents are that jumping spiders and parasitoid wasps can orient to the extremely diverse, and one major theme in the study of signals of vibrationally communicating insects. vibrational communication is how the substrate influences Theabsence of a private channel can be appreciated by the evolution of vibrational communication systems. listening to vibrational soundscapes in which multiple There are two general issues: first, how do the vibration- individuals and/or species are signaling at the same time. transmitting properties of the substrate influence the evo- Chorusing has been documented in leafhoppers and tree- lution of signalers and receivers using that substrate? And hoppers living at relatively high densities on plants. During second, how do the sources of vibrational noise influence chorusing, stationary, signaling males produce signals for the evolution of signals and signaling behavior? These extended periods, usually alternating signals with each other aspects of the vibrational modality have been best studied (Figure 4; signal example 2). Other forms of coordinated for signals transmitted through living plants. signaling interactions among multiple individuals occur in It has been hypothesized that animals using living group-living treehoppers (see section ‘Functions of Vibra- plants to communicate should produce broad-band sig- tional Communication’) . The vibrational soundscapes of nals, ensuring that at least some frequencies are trans- living plants may also transmit a wealth of signals from mitted to receivers. The rationale is that there is such different insect species communicating at the same time great variability in the vibration-transmitting properties (Figure 5; signal example 3).

(kHz) Frequency

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Figure 4 A chorus of leafhoppers, with males signaling in alternation. This is an unidentified species (four males shown in photo inset) recorded at Tiputini Biological Station, Ecuador.

Frequency (kHz)

2468101214

Time (s) Figure 5 A complex vibrational soundscape with three or more species signaling on the same small (<1 m tall) plant. No signalers were identified in this recording, which was made near Gamboa, Panama.

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502 Vibrational Communication of living plants – the frequency spectrum of a signal varies wind-induced noise might be important for some species substantially, and often unpredictably, with distance from and unimportant for others (e.g., species signaling on the signaler – that specialization on a single, optimal plants in sheltered locations). Second, even if wind is frequency is unlikely to function well. This hypothesis important for most species, the properties of wind- has been influential but has never been formally tested, induced noise might differ from plant to plant, especially although studies of wolf spiders show that their broad- in the amount of energy present in different frequencies. band, percussive signals are successful in courtship on Wind noise has only been characterized in a few plants; in multiple substrates. It is clear, however, that it does not one case, two structurally different plants were found to applyto all species, because although many vibrationally have different frequency spectra of wind-induced vibra- communicating species do produce broad-band signals, tions, while in another, two structurally similar species of many others produce tightly tuned signals, with most woody plants had very similar profiles. At present, it is not of their energy concentrated in a very narrow range of possible to say whether wind imposes similar selection on frequencies. vibrational signals (e.g., selecting for higher frequencies There are relatively few studies of vibration trans- that avoid those present in wind noise) or whether it may mission in plants, and fewer still that have characterized favor the use of different signals for efficient communica- morethan one or two examples of a given host plant. tion on different plants. For most studies, there is little information about which Whether or not the presence of wind influences the plant parts are used by signalers in nature, or about the evolution of signal frequency, as a major source of noise in properties of more than one host species for organisms the vibrational channel, it is very likely to influence the that use many different host species for communication. signaling behavior of organisms. One way for organisms to Study of hosts used by the cosmopolitan green stink bug deal with wind noise is spatial avoidance or communica- reveals that several of the plants it uses transmit vibration in relatively wind-free environments. Such environ- tions in the 100-Hz range most effectively, suggesting that ments as the forest interior are characterized by lower signals of pentatomid bugs are adapted to this ‘frequency wind speeds; however, for plant-feeders, the most nutri- window.’ In contrast, for the host plants used by some tionally valuable plant tissues are usually those in high- signaling treehoppers with narrowly tuned signals, the light environments, which are, of course, less sheltered. As optimal frequency varies both between host species and a strategy for avoiding wind noise, then, spatial avoidance between modules (such as stems vs. leaves) within the of wind may not be available to many species. plant.For two closely related treehoppers using different Temporal avoidance of wind can occur at two scales. plant species and different modules (woody stems vs. First, often there are predictable daily patterns of rise and leaf petioles), signal frequency has diverged to match fall in wind velocity. Males of at least one treehopper the contrasting vibration-transmission properties of their species do signal more often during morning and evening typical substrate. hours when wind speeds are lower in its forest edge habitat, but whether this pattern has evolved specifically in response to wind is unclear. Second, wind speed is often Sources of Noise in the Vibrational Channel quite variable over a scale of minutes or seconds, and Windis the major abiotic source of noise in living plants, organisms could use gap detection to signal during short and probably in other substrates such as leaf litter. As wind-free periods. For one treehopper, laboratory experi- anyone who has tried to record plant-borne vibrations ments show that males signal during brief wind-free gaps. outdoors can attest, the air is seldom completely still. How This avoidance of signaling during wind gusts is likely do organisms communicating with plant-borne vibrations important for communication; females responded less to deal with the pervasive noise generated by wind? Wind has male signals masked by wind, especially when the signals the potential to be a major influence on the evolution of were low in amplitude. vibrational communication systems, influencing the evolu- In addition to wind, rain is a significant source of tion of signal form, signaling behavior, or both. vibrations for living plants, leaf litter, and probably for

The most obvious way in which wind could influence any exposed substrate. In plant leaves, the impact of the evolution of vibrational signals is by selecting for the araindropcausesaninitialhigh-amplitude,broad- use of frequencies that avoid masking by those present in band pop, with a decreasing tail of lower frequencies. the wind. In living plants, most of the energy in wind- Ahardrainfalllikelyprecludescommunication,asdoes generated noise is in low frequencies, less than 100 Hz. heavy wind. But in environments subject to frequent Lower wind velocities cause swaying and low-frequency low-intensity rainfall, organisms likely have adaptations vibrations, while higher velocities cause leaves to flutter that enhance communication. and stems to strike each other, exciting a broader Airborne sounds are another source of noise in spectrum. There are at least two ways in which wind the vibrational channel. Leaves vibrate in response might exert an influence on signal evolution. First, to airborne sound, and recordings made in natural

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Vibrational Communication 503 environments include not only the signals of vibrationally alerting the mother to the arrival of a predator. Predator communicating species but also the signals of nearby alarm signaling also occurs in some rodents, although here, species signaling with airborne sound, such as cicadas it is the parents that signal to alert the offspring. and birds. The significance of these induced vibrations Vibrational signaling is important for other social and for communication is unknown, but in some cases, they ecological relationships as well. Some caterpillars defend may provide useful information; for example, a wolf spi- leaf territories using a repertoire of vibrational signals. For der was shown to alter its behavior in response to induced lycaenid and riodinid caterpillars, and for some treehop- vibrations from the songs of potential avian predators. pers, vibrational signals facilitate the attraction of ant

Finally, a source of noise for one species may be an mutualists or ant detection of potential predators. important cue for another. The vibrations produced by wind blowing through mounds of grass are potential cues for foraging golden moles in their sand dune habitat, Recording and Playback Methods for and the ground-borne rumbling of distant thunder may Studying Vibrational Communication be used by elephants to locate areas where rain has recently fallen. What follows is a discussion of methods for vibration

recording and playback that have been used extensively for vibrations transmitted through living plants, but much Functions of Vibrational Communication will be relevant to other substrates.

There are many applications for vibration measure- Sexualselection is the major engine of diversity in the ment in engineering, manufacturing and testing, and the evolution of animal signals. The vibrational signals of music industry. As a result, there are many options avail- insects and spiders provide a remarkable panorama of able for detecting and recording vibrational signals. These the historical action of sexual selection, given the ancient methods range widely in cost and suitable applications. nature of this communication channel, and the hundreds The gold standard is the laser vibrometer, which uses of thousands of living species that use it. Doppler shifts in reflected laser light to measure the

Evidence of the importance of sexual selection in the velocity of a moving surface (analogous to the use of diversification of vibrational signals and in speciation comes radar for measuring vehicle speed). The day-to-day work- primarily from the study of insects, especially lacewings, horse is the accelerometer, which is attached to the vibrat- stoneflies, and the Auchennorrhyncha (planthoppers, leaf- ing substrate with wax or adhesive and has an output hoppers, and treehoppers). All of these groups contain proportional to the acceleration component of the signal. sibling species, close relatives that are phenotypically simi- Newer technology includes piezoelectric film, which has lar except in mating signals and preferences. In the lacew- high sensitivity when used with appropriate amplifiers, ings, for example, systematic study has revealed unexpected but has not been widely used. Other methods arise from acoustic diversity within what were thought to be single the music industry, including phonograph cartridges and species, and experimental research has implicated sexual piezo pickups; these are often convenient, of low-cost, and selection as the evolutionary force driving both song diver- sensitive, but have disadvantages for some research pur- sification and species formation. Important work on sexual poses. Table 1 provides a comparison of some common selection is also being conducted in spiders, where vibra- methods of recording vibrational signals. tional signals are often components of multimodal mating One general issue is the extent to which the measuring displays that include motion, color, and substrate vibra- method alters the properties of the substrate, and as a tion. These multimodal signals are especially diverse in result of the transmitted signal. This ‘mass loading’ issue jumping spiders and wolf spiders. varies in importance depending on the size of the sub-

Vibrational signals are used not only in mating but also strate and the importance of making precise measure- in communication among members of social groups. In ments of signal properties and/or of substrate effects on contrast to sexually selected signals, which are often com- those properties. plex and rapidly evolving, social signals are usually rather Vibrational playbacks are possible using a wide variety simple, with their structure evolutionarily conserved of methods, compared in Table 2. The most common among closely related species. In the eusocial insects, vibra- playback devices include a shaker, specifically designed tion is important in alarm communication in termites and for coupling a vibration to a substrate; a magnet attached some ants, and in recruitment to profitable food resources to the substrate and driven by sending the signal through in other ants. In noneusocial insects, such within-group an electromagnet placed in close proximity; and modifica- communication has been best studied in group-living tions of other technology, such as removing the membrane immatures of sawflies and treehoppers. Vibrational signal- from a loudspeaker and coupling the movement of the coil ing among group members is important for remaining in a to the substrate using a pin. Any of these methods can group, finding food, and, in species with maternal care, work well, but their characteristics vary widely.

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Table 1 Methods of recording substrate-borne vibrational signals

Physical Recording property Substrate transducer measured Frequency response Sensitivity Repeatability of measurements loading Field use Costa

Laser Velocity Flat over large range Excellent High None Limited to portable $$$$$+ vibrometer versions and windless conditions Accelerometer Acceleration Flat over range Good/very good High Moderate Well suited, easy to use $$$ $$$$ À and signal determined by conditioner resonant frequency Piezo film Strain Flat w/respect to strain Excellent Good if proper attachment can be achieved; Low Yes, though depending $$$

transducer if attached properly output may be substrate specific in terms of on size and shape

and amplifier relating measures to velocity or attachment may be

acceleration an issue Piezo pickup Acceleration Unknown Fair Untested Moderate Well suited (e.g., if $$ $$$ À and amplifier mounted on clip) Ceramic phono Displacement Far from flat, may Excellent Low; fine for detecting signals and measuring Low Yes, but requires $$ $$$ À cartridge depend on gross-temporal features precise positioning and amplifier placement aCost (USD): $$ = 10s; $$$ = 100s; $$$$ = 1000s; $$$$$ = 10 000s.

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Table 2 Methods of playing back substrate-borne vibrational signals

Repeatability of Output playback Playback device proportional to Frequency response characteristicsa Field use Costb

Modified Velocity Not flat Not tested Yes $$ loudspeaker Shaker Acceleration/ Well defined; for some High Yes $$$ $$$ À may depend shakers response is flat on frequency w/respect to

range acceleration

Magnet/ Not tested Determined by various Low Yes $$ electromagnet factors including distance between magnet and electromagnet Piezo actuator Acceleration Well defined, usually flat High Yes $$$$ and driver over range determined by resonant frequency aNote: all playback methods can yield repeatable results if the proper compensation procedure is used to ensure the correct amplitude and frequency response (see text for explanation). bCost (USD): $$ = 10s; $$$ = 100s; $$$$ = 1000s; $$$$$ = 10 000s.

There is one basic requirement in conducting vibra- See also: Cooperation and Sociality; Group Living; tional playbacks: to ensure that the vibrational playback Mating Signals; Parent–Offspring Signaling. signal has the proper characteristics at the location of the experimental subject, it is necessary to compensate for changes introduced into the signal by the substrate and Further Reading by mismatches in the amplitude–frequency response of the recording and playback devices. Simply recording a vibrational signal and playing it back can result in severe Barth FG (2002) Spider senses – Technical perfection and biology. Zoology 105: 271–285. changes in the signal by the time it reaches the experi- Cocroft RB and Rodriguez RL (2005) The behavioral mentalanimal. In contrast, if the experimenter compen- ecology of insect vibrational communication. BioScience 55: sates for the filtering imposed by the equipment and 323–334. Cokl A and Virant-Doberlet M (2003) Communication with substrate- substrate, high-fidelity vibrational playbacks are possi- borne signals in small plant-dwelling insects. Annual Review of ble with any of the methods mentioned earlier. The basic Entomology 48: 29–50. procedure is to calculate that filter and apply an inverted Hill P (2008) Vibrational Communication. Cambridge: Harvard University Press. form of it to the playback stimuli. Although the playback Narins PM (2001) Vibration communication in vertebrates. In: Barth FW of vibrational signals is slightly more difficult to execute and Schmid A (eds.) Ecology of Sensing, pp. 127–148. Heidelberg: properly than that of airborne sound, it provides a pow- Springer-Verlag. O’Connell-Rodwell C (2008) The Elephant’s Secret Sense: erful method of hypothesis testing that works extremely The Hidden Life of the Wild Herds of Africa. Chicago: University of Chicago Press. well with a wide range of species.

Encyclopedia of Animal Behavior (2010), vol. 3, pp. 498-505