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Stealth percussionists of the animal world

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Animals may not be able to predict earthquakes, but many—from elephants to spiders—are quite adept at detecting vibrations that are imperceptible to humans.

Yes, there’s a whole world out there we are mostly unaware of. It jiggles and gyrates and shakes and vibrates as waves travel through solid substrates such as sand and tree trunks. Eventually, vibrations reach structures in animals that evolved to detect such vibrations, including oversized ear bones, crystal-filled sacs, and strain-sensing exterior membranes. Critters emitting these signals use them to convey information about such things as lurking predators, food sources, and potential mates; they do so by movements including drumming on surfaces, rubbing stuff together, and shaking their booties—or abdomens.

But while these substrate-borne vibrations form the lifeblood of many sensory systems, most are imperceptible to even the most observant person. Indeed, everything around us is vibrating, from plants and trees to houses and sidewalks. Merely stepping into a garden produces vibrations detectable by thousands of animals—and by the instruments scientists use to eavesdrop on this wiggling world.

The study of vibration communication is gaining momentum as scientists realize just how ubiquitous it is. But why is it taking so long to catch up with other sensory systems? "It’s really been ignored because we can’t detect it," said U.C. Berkeley biologist Damian Elias, who studies spiders. "This type of sense is totally foreign to the experience of being human."

How do vibrations inform the human experience? Well, earthquakes are a catastrophic form of substrate vibration, as we’ve seen all too clearly. On a smaller scale, many of us set our cell phones to "vibrate" every now and then. (But can you actually feel the vibrations from the phone when it’s on a surface, or do you mostly listen for the tell-tale clatter?) We do feel the rumbling of transiting trains and may startle at a dryer’s "spin" cycle shaking the house, and most of us have probably been unfortunate enough to stop at a red light next to some dude thumping the bass in his car – and in ours, temporarily. But we mostly go through our days without noticing these often-subtle vibrations. "So much is happening that we can’t detect," Elias says.

It’s safe to say that vibration detection in animals far surpasses our own.

Because we’re vibrationally-challenged, scientists use a variety of tools to translate seismic waves into audible sounds. These instruments include modified phonographs, geophones – which convert ground movement into sound – and laser Doppler vibrometers, which use focused laser beams to measure substrate wiggles. To play animal vibrations into ground, scientists borrow gadgets from the booming home entertainment industry: sound transducers that normally make cars and houses bump around. Then they bury the hardware before playing the calls of the wild.

Now, scientists suspect that more than 200,000 insect and arachnid species use seismic communication systems, including crickets, katydids, spiders, and scorpions. Crustaceans do, too. Amphibians? Definitely. Frogs are among the most sensitive vertebrate vibration detectors on land. Reptiles, such as snakes and lizards, also join the ground-sensing group. So do our hairy mammalian relatives, from the very big to the very small.

Here is a smattering of critters using this seismic sense for the equivalent of everything from restaurant scouting to intruder detecting to internet dating:

Jumping spiders Salticidae: The Music Men

For years, scientists considered male jumping spiders to be among the flashiest of arachnids, dazzling females with colorful, dancing courtship displays. But then they noticed the males’ abdomens moving while they performed their seductive, leg-flinging moves – and thus became curious about whether vibrations accompanied their already virtuosic performances.

Rejiggering a phonograph needle to transduce sound from a vibrating surface allowed then-graduate student Damian Elias to detect the spiders’ hidden secrets. Surface vibrations produced during a male’s courtship routine were translated into audible sound, which Elias then listened to. "We were very surprised," Elias says, of hearing their early recordings. "They were not only making these vibrations, but they were incredibly elaborate, arguably as elaborate as the visual displays." Indeed, it appears these spiders are very much like flamenco dancers or a one-man band: they sing and clap and stomp and dance, using their abdomens and legs to produce a mixture of hums, drums, and snaps. (see videos on website, too!)

Now, with a well-equipped lab of his own, Elias has recorded the vibrations of around 60 jumping spider species using a laser Doppler vibrometer. "You can listen to the song and know exactly which species it is," he says. He likens routines within a species to jazz tunes, with a known structure and melody, but with room for improvisation and extended instrument solos. Females detect the vibrations using exoskeletal sensory structures called "slit sensilla," which are basically cracks covered by a strain-sensitive membrane. How does Elias know females are paying attention to the vibrations and not just the visual display? "If you experimentally manipulate the male’s ability to produce vibrations," he says, "The females are less likely to accept males as a mate, and more likely to eat them."

Kangaroo rats Dipodomys: Tiny dancers, tap-dancing in the sand

Like their namesake, these solitary rodents hop on two legs. But the back two are often working to drum out patterns of "footrolls" in the dirt – yes, kangaroo rats are accomplished tap-dancers, and they use footdrumming to communicate with their neighbors, sending vibrations through the ground and into the air.

The most complex sequence of studied footdrumming belongs to the Banner-tailed kangaroo rat (Dipodomys spectabilis), a resident of the arid U.S. Southwest. Each of these furry mound-dwellers marches to a different drummer, producing a unique footroll—a series of thumps—that it uses to guard its cache of seeds. Mounds can be up to 10 meters apart, and kangaroo rats drum both on top of and inside their burrows, suggesting that footdrumming is of both airborne and subterranean importance.

By keeping their tap-dances constant, the rats can easily tell who’s a neighbor and who’s an intruder, preventing costly skirmishes. But what if they relocate? The kangaroo rats learn new choreography. "They alter their drumming pattern to be different from their neighbors," says behavioral ecologist Jan Randall, who worked out the kangaroo rats’ communication system.

In addition to preventing fights among neighbors, kangaroo rats use their fleet footwork to signal their awareness of predators (snakes, mainly), and to compete for mates.

Randall also studied the Giant (D. ingens) and Desert (D. deserti) kangaroo rats and found that their footrolls were species-specific. As well, they didn’t share their cousin’s facility for improvisation and learning new steps – no identifiable individual variation — but they all stomped around for the same reasons.

Here are two recordings from Jan Randall, one of footrolls among banner-tailed kangaroo rat individuals, and the other of giant kangaroo rats:

Banner-tailed Kangaroo Rats:

Bannertail 

Giant Kangaroo Rats:

Giant Kangaroo Rat 

Namib desert golden mole Eremitalpa granti namibensis: Is just really frikkin’ cute.

This blind, nocturnal extremely adorable furball lives in the Namib desert. During the day, the golden mole keeps cool by hiding under the sand. In the evenings, it can travel more than 5 kilometers while searching for its favorite tasty treat: termites. Along with 99% of the desert’s biomass, termites live near grassy mounds called "tussocks." When desert winds blow through the grass, they set the tussocks into subterranean resonance – and a hungry golden mole uses these vibrations to guide the first part of its nightly excursion. "The mound is a seismic beacon in the Namib desert," says U.C.L.A. neuroethologist Peter Narins, who, with colleagues, demonstrated that goldens use vibrations to guide their termite tracking.

As the sandy traveler nears the tussock, it’s able to detect the more subtle vibrations of the termites themselves, and it sneaks up to claim its crunchy snack. Sometimes, if the golden mole is lucky, it might get something bigger and better – like a cricket.

How do the goldens sense these incredibly subtle vibrations? According to Narins, the moles are "mostly malleus." The malleus is a middle-ear bone—humans have it, too—that moves in response to seismic signals, and it is abnormally large in these golden cuties (with a ratio of malleus to body mass that is roughly 5600 times greater than a human’s). Using their enormous middle ear, golden moles can hear vibrations under the sand—as long as their ears are buried and in contact with the substrate. They use a behavior called "head-dipping" to accomplish this, literally burying their heads every few steps to stay on course. (see video!) Narins says there are still questions to be answered about the golden mole, though, and hopes they might provide a model for earlier earthquake detection. "If a device could mimic the golden mole’s middle ear and detect very low-level vibrations," he says, "It might be useful for detecting earthquake precursors."

Puerto Rican white-lipped frog Leptodactylus albilabris: Thumps in a bog

Perhaps the best-known of the amphibian thumpers, the Puerto Rican white-lipped frog sprang to notice when Peter Narins and UC Berkeley neurobiologist Edwin Lewis teamed up to sort out its seismic secrets. While attempting to record audible calls from the ground-dwelling, nocturnal frog, Narins noticed that it stopped vocalizing whenever he approached – even when he tiptoed. They hypothesized that the frog detected vibrations from distant footsteps, and got to work solving the riddle of the frog’s super-sensitivity.

Together, they determined that the Puerto Rican white-lipped frog’s freakish seismic sensitivity results from an inner ear sac brimming with calcium carbonate crystals. Extremely subtle vibrations shake the rocky gems, and they in turn excite cells that produce nerve impulses. And thus the frog perceives the far-away footsteps, stops singing, and complicates field recordings.

"But a seismometer as sensitive as that of the white-lipped frog must have some function other than detecting the presence of researchers," Narins wrote. [1]

So he and Lewis went back into the field, this time armed with geophones — instruments that record ground vibrations and turn them into perceptible sound. They found that each time the males call, they produce a seismic "thump" when their vocal pouch expands and crashes into the ground. Males in the area sense these thumps and respond, using calls both to attract females and distance themselves from other males. Lewis and Narins recorded these thumps and played them to frogs using electric typewriter parts that had been reconfigured for the noble purpose of emitting fake frog vibrations. The result? Males within three meters of the pseudo-amphibian unleashed a chorus of song in response to its call.

But despite that result, the frog’s dependence on vibration communication is still murky. "My sense is that white-lipped frogs may turn to their seismic sense for chorusing with neighbors when the ambient airborne noise is loud enough to block the auditory channel," Lewis says. "It is clear that about half of the calling white-lipped frogs are not generating seismic signals at all. It is not clear that the other half are generating seismic signals deliberately."

[1.] "Frog Communication," Scientific American, 1995

Treehoppers Membracidae: The Stems are Zinging with the Songs of Insects

Plant-loving, often communal-living, and well-armored, treehoppers manage to pack an enormous amount of variety into a small package, reaching a maximum length of just 2 centimeters. There are more than 3,000 species of these little stem-clingers, who often look like thorns or brambles due to their highly camouflaged – and sometimes extremely bright – coloration. Some species are solitary. Others live in tightly clustered family groups with prolonged periods of maternal care.

Treehoppers communicate with one another by vibrating the stem they’re parked on, using mechanisms that involve abdominal movements and a structure that might resemble the cicada’s noise-maker. None of their signals are perceptible by humans, so scientists record them using instruments that translate stem vibrations into audible sounds. They found that treehoppers produce a startling variety of vibrational songs, with some sounding—to our ears—like whistles, underwater voices, or staccato pulses. (listen here)

When do they make their music? For starters, males advertise their presence to females with their own unique mating vibration; if the female is interested, she’ll vibrate back. Describing this interaction in Costa Rican thornbugs (Umbonia crassicornis), University of Missouri biologist Rex Cocroft writes [1], "The male vibrates his abdomen to create a rich, bubbling down-sweep of tone and percussion that courses through the plant. The call could perhaps be imitated by a skilled duo of French horn and snare drum." He continues, "If a receptive female is nearby, she responds with a low vibrational growl."

But symphonic calls don’t only accompany romantic overtures: treehopper nymphs will signal when they’ve found a new stem to munch on; and, when nymphs are part of a family group, they’ll produce a joint alarm signal in response to a predator, seeking help from mom. "The most unique aspect of vibrational communication in treehoppers is their use of vibrational signals in social interactions," Cocroft says.

[1.] "Thornbug to Thornbug," Natural History Magazine, 1999

Elephants Loxodonta/Elephas: The nose knows…and the toes.

These big-eared, trumpeting mammals need no introduction. For years, scientists have known their calls contain low, sub-sonic rumbling frequencies. But elephant vocalizations also shake the ground. The enormous pachyderms detect vibrations through their nose and their toes, locating the shaking source using a combination of sensory structures and jiggling bones.

Caitlin O’Connell-Rodwell began to suspect elephants sensed vibrations when she noticed them striking some of the same "listening" postures as the seismic-sensing insects she’d studied. "I could see there was a pattern," says O’Connell-Rodwell, an ecologist at Stanford University, who observed the postures in response to approaching herds or vehicles. "They’ll place the tips of their toes on the ground, or lift up a foot. Sometimes they’ll lean forward kind of dramatically, also with the trunk on the ground."

To test whether elephants sent and received seismic signals, O’Connell-Rodwell recorded their rumblings and played them back to groups of pachyderms, using what’s called a "butt-kicker." "It’s a great, great device for us," she says of the gizmo normally used in home entertainment systems – and likely in that dude’s boom-car as well. "We buried them in the ground and broadcast the elephant calls."

Then she watched while elephants responded to the underground songs. Alarm calls, contact calls, mating calls—they all carry information seismically.

Now, O’Connell-Rodwell is trying to figure out which pathways elephants use to sense the vibrations. They appear to prefer bone conduction, she says, which is enhanced by balancing one foot on tip-toe perpendicular to the sound source. Ground sound vibrates the toe bone and travels up through the leg, before eventually rattling the middle ear. Pressing their trunk on the ground may help elephants triangulate the vibrations’ source, she adds.

It’s possible that elephants can sense vibrations coming from as far as 10 miles away. But it’s hard to test, O’Connell-Rodwell says, "because there’s so much human-generated noise in the ground."

For further reading:

The Use of Vibrations in Communication: Properties, Mechanisms, and Function across Taxa. (2011) Ed: Caitlin O’Connell-Rodwell; includes chapters written by scientists featured in this post.

Image credits: 1. Male jumping spider, Habronattus dossenus, in courtship posture. Image: Damian Elias; 2. Courting jumping spider. Image: Tamas Szuts; 3. Banner-tailed kangaroo rat. Image: Jan Randall; 4. Giant kangaroo rat. Image: Jan Randall; 5. Namib desert golden mole. Image: Galen Rathbun, California Academy of Sciences; 6. Puerto Rican white-lipped frog. Image: USGS; 7. A courting pair of Campylenchia latipes (Columbia, MO). Image: Rex Cocroft; 8. Newly eclosed adults of Metcalfiella monogramma, Mexico. Image: Rex Cocroft; 9.Ceresa taurina. Image: Bruce Marlin; 10. An elephant strikes a seismic sensing stance. Photo: Caitlin O’Connell-Rodwell; 11. Male elephants, such as this one, "listen" to calls from females in estrus with their feet and trunks. Photo: Caitlin O’Connell-Rodwell.

References:

Jumping spiders

Elias D.O., Mason A.C., Maddison W.P., and Hoy R.R. (2003) Seismic signals in a courting male jumping spider (Araneae: Salticidae) The Journal of Experimental Biology 206, 4029-4039.

Elias, D.O., Sivalinghem S., Mason, A. C., Andrade, M. C. B., and Kasumovic, M. M. (2010) Vibratory communication in the jumping spider Phidippus clarus: Substrate-borne courtship signals are important for male mating success, Ethology 116: 990-998

Elias, D. O., Hebets, E. A., Hoy, R. R., Maddison, W. P., and Mason, A. C. (2007). Regional song differences in sky-island populations of Habronattus pugillis Griswold. Journal of Arachnology, 34 (3): 545-557.

lias, D. O., Hebets, E. A., Hoy, R. R. and Mason, A. C. (2005). Seismic signals are crucial for male mating success in a visual specialist jumping spider (Araneae: Salticidae). Animal Behaviour, 69 (4), 931-938.

Kangaroo rats

Randall, J.A. (1993) Behavioural adaptations of desert rodents (Heteromyidae). Animal Behaviour 45, 263-287.

Randall, J.A. (1994) Convergences and divergences in communication and social organisation of desert rodents. Australian Journal of Zoology 42, 405-433.

Randall, J.A. (1997) Species-specific footdrumming in kangaroo rats: Dipodomys ingens, D. deserti, D. spectabilis. Animal Behaviour 54(5): 1167-75.

Randall JA, Lewis ER. (1997) Seismic communication between the burrows of kangaroo rats, Dipodomys spectabilis. Journal of Comparative Physiology A. 181(5):525-31.

Namib desert golden mole

Fielden, L.J., Perrin, M.R. & Hickman, G.C. (1990) Feeding ecology and foraging behaviour of the Namib Desert golden mole, Eremitalpa granti namibensis (Chrysochloridae). Journal of Zoology, London 220:367-389.

Lewis ER, Narins PM, Jarvis JU, Bronner G, Mason MJ. (2006) Preliminary evidence for the use of microseismic cues for navigation by the Namib golden mole. The Journal of the Acoustical Society of America 119(2):1260-8.

Narins PM, Lewis ER, Jarvis JJ, O’Riain J. (1997) The use of seismic signals by fossorial southern African mammals: a neuroethological gold mine. Brain Research Bulletin 44(5):641-6.

Willi, U. B., Bronner, G. N. & Narins P. M. (2005) Middle ear dynamics in response to seismic stimuli in the Cape golden mole (Chrysochloris asiatica). Journal of Experimental Biology 209: 302-313.

Puerto Rican white-lipped frog

Lewis, E.R. and Narins P.M. (1985) Do Frogs Communicate with Seismic Signals? Science 227(4683): 187-189.

Lewis E.R., Narins P.M., Cortopassi K.A., Yamada W.M., Poinar E.H., Moore S.W. and Yu X. (2001) Do male white-lipped frogs use seismic signals for intraspecific communication? American Zoologist 41(5): 1185-1199.

Lopez P.T., Narins P.M., Lewis E.R., and Moore S.W. (1988) Acoustically induced call modification in the white-lipped frog, Leptodactylus albilabris. Animal Behaviour 36(5): 1295-1308.

Treehoppers

Cocroft, R.B. (1999) Parent-offspring communication in response to predators in a subsocial treehopper (Hemiptera: Membracidae: Umbonia crassicornis). Ethology 105, 553-568.

Cocroft RB. (2005) Vibrational communication facilitates cooperative foraging in a phloem-feeding insect. Proceedings of the Royal Society B 272(1567):1023-9.

Cocroft RB, Tieu TD, Hoy RR, Miles RN. (2000) Directionality in the mechanical response to substrate vibration in a treehopper (Hemiptera: Membracidae: Umbonia crassicornis). Journal of Comparative Physiology A 186(7-8):695-705.

Rodríguez RL, Sullivan LE, Cocroft RB. (2004) Vibrational communication and reproductive isolation in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). Evolution 58(3):571-8.

Sullivan-Beckers L, Cocroft RB. (2010) The importance of female choice, male-male competition, and signal transmission as causes of selection on male mating signals. Evolution 64(11):3158-71.

Elephants

O’Connell-Rodwell CE, Arnason B, Hart LA. (2000) Seismic properties of elephant vocalizations and locomotion. The Journal of the Acoustical Society of America 108: 3066–3072.

O’Connell-Rodwell CE, Hart LA, Arnason BT. (2001) Exploring the potential use of seismic waves as a communication channel by elephants and other large mammals. American Zoologist 41: 1157–1170.

O’Connell-Rodwell CE, Wood JD, Rodwell TC, Puria S, Partan SR, Keefe R, Shriver D, Arnason BT, Hart LA. (2006) Wild elephant (Loxodonta africana) breeding herds respond to artificially transmitted seismic stimuli. Behavioral Ecology and Sociobiology 59: 842–850.

O’Connell-Rodwell CE, Wood JD, Kinzley C, Rodwell TC, Poole S, Puria JH. (2007) Wild African elephants (Loxodonta Africana) discriminate between familiar and unfamiliar conspecific seismic alarm calls. The Journal of the Acoustical Society of America 122(2) 823-830.

O’Connell-Rodwell CE. (2007) Keeping an "ear" to the ground: seismic communication in elephants. Physiology 22:287-94. Review.

About the Author: Nadia Drake is a student in the Science Communication program at the University of California, Santa Cruz. She earned a PhD in genetics from Cornell University and has spent years climbing trees and performing as a professional ballet dancer. Nadia loves geeking out about science, wearing silly costumes, and writing about planets and animals—and everything in between, especially if it involves an adventure. She’s interned at the Santa Cruz Sentinel and the San Jose Mercury News, and will begin an internship with Nature next week. Nadia blogs at A Tale of Ten Slugs and tweets as @slugnads.

The views expressed are those of the author and are not necessarily those of Scientific American.






Comments 5 Comments

Add Comment
  1. 1. CoolerThanAbsoluteZero 3:39 pm 03/22/2011

    I’ve made a few beats with animals and hunters in mind; Troglodyte’s Trance (Cave Rave Edit) and Apex Alpha Agressor (Animal Kingdom Edit). Please have a listen on http://www.soundcloud.com/jwh-2 on page 2 and 5 in the track listing, and you can download all my beats for free in .mp3. Thanks for listening and enjoy.

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  2. 2. JDahiya 5:09 am 03/23/2011

    Thank you, Nadia Drake! One of the most fascinating articles I’ve read (and seen and heard) in months. Keep them coming! The spider dance is amazing, and the treehopper sounds are diverse and unexpected. Who’d have thought insects, frogs and elephants have so much in common?

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  3. 3. jtdwyer 1:44 pm 03/23/2011

    Excellent article – a real tactile experience!

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  4. 4. Nadia Drake 11:22 pm 03/24/2011

    Thank you! So glad you enjoyed this piece — I had a great time putting it together.
    Cheers!
    n

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  5. 5. Bora Zivkovic 10:48 pm 04/5/2011

    Also see recent Q&A that Nadia Drake conducted with Dr.Peter Narins about the golden moles: http://scicom.ucsc.edu/Q&A/2011/narins.php

    Link to this

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