From the outside, plants seem to be the silent inhabitants of a noisy planet. But this impression is deceptive. Plants harbor an alien world of animal signals—eerie vibrational songs transmitted through stems and leaves by insects, spiders, and even some frogs and lizards. In fact, so many species send messages through plants that these songs may outnumber all other animal sounds on Earth. Eavesdropping on this hidden world is revealing many surprises, including communication between some insect mothers and their offspring.
For the past seven years, I have been listening to treehoppers, often bizarrely shaped insects in the family Membracidae. One species, the thornbug (Umbonia crassicornis), is common in Costa Rica’s San Luis Valley, on the western slope of the Cordillera de Tilarán, where patches of montane forest mix with abandoned pastures that are gradually being reclaimed by trees. Young acacia and guanacaste trees rise out of thigh-high star grass, providing ideal thornbug habitat. The insects spend most of their lives clinging to the stem of a sapling, piercing the bark near a growing tip and sucking up sap with mouthparts that work like a flexible syringe.
With a hard shell that resembles a half-inch rose thorn, adult thornbugs can easily be mistaken for part of the plant they cling to. The spiky similarity goes beyond looks: an elongated wedge with a sharp point at each corner, the shell also serves as protective armor. If you’re not careful, picking up a thornbug can feel like getting stuck by a burr.
Up close, an adult thornbug is a colorful sight: lime green with orange lines radiating from a red-tipped spine (newly emerged adults are bright yellow). From a distance, though, these treehoppers blend into the background. The female is especially difficult to spot, often hidden beneath a spray of delicate, light green leaves or visible as little more than a spiny interruption on the gradually tapering stem.
Adult males are more likely to attract attention as they fly from plant to plant in search of females. After landing, 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. A person watching the male would notice only a silent, blurred movement of the abdomen, but headphones and a vibration microphone (contained in a fingernail-sized aluminum cube that can be clipped right onto a stem) can pick up the call and convert it into airborne sound discernible to human ears. If the male receives no answer, he flies to another plant and calls again. If a receptive female is nearby, she responds with a low vibrational growl, after which the pair engages in a duet while the male locates her.
After mating, the female inserts a hundred or so cream-colored eggs into the bark, laying them in two curved rows that look like a pair of parentheses. She then begins the parental care that will consume her remaining six weeks of life. For the first two weeks, she straddles the eggs to protect them from parasites. Just before the eggs hatch, she again inserts her ovipositor into the stem, this time to create a series of slits that spiral around it for an inch or so below the egg mass. When the nymphs emerge, each the size of a sesame seed, they line up along these ready-made feeding holes. The mother then takes up a position on the stem just below her offspring, poised to defend them or to cut additional feeding slits as needed. She also intercepts any nymph that starts to walk away; a few strokes with her foreleg generally cause the wanderer to turn around and return to the group.
With a steady source of food assured, the nymphs’ main challenge is to avoid being eaten for the next month, the time it takes to grow to adulthood. By two weeks of age, they encircle the stem in a tightly packed group with the bumpy, slightly prickly texture of a pineapple. Though they lack the hard shells of adults, these pea-sized triceratops are armed with a trio of spines behind the head, as well as with bright red eyes and red, white, and black bodies to advertise their distastefulness. Yet this is still not enough to discourage all predators. In the San Luis Valley, the most dangerous one is Pseudopolybia compressa, a compact, matte-black wasp as big as an adult female thornbug and three times the size of a nymph. Once attacked by a wasp, the only thing the nymphs can do is call for help from the individual most invested in their survival: their mother.
As a wasp closes in, the nearest nymphs make a brief vibration that sounds, when converted for human ears, like “ch.” This starts a chain reaction as neighboring nymphs, sensing the vibration through their legs, respond immediately with “ch” signals of their own. The wave of signaling spreads in a flash, and the signals of the whole group pile up into one collective vibrational shout. Heard through headphones, these group efforts sound as if someone has tuned a radio to the static between stations and then flicked the volume from zero to maximum and back again every second or so.
Alerted that her offspring are in danger, the mother moves to their defense. Lacking bite, sting, or chemical spray, however, the female has little in the way of offensive weaponry. Her most potent weapons are vigilance and the ability to deliver a powerful kick with her club-shaped hind legs. She walks across the nymphs’ backs, approaches the wasp, and lifts her hind legs off the surface, ready to kick. In response, the wasp circles the stem in an erratic orbit, jerking away slightly as the female fans her wings, then returning to a different part of the cluster of nymphs. The standoff may continue for several minutes.
Sometimes the wasp is discouraged by the mother’s harassment and flies off. But often, while the female is in one part of the group, the wasp lands in another and grabs a nymph-usually one at the margins of the cluster-with its mandibles. As the wasp tugs, the nymph clings to the stem with all six of its legs while its siblings continue to produce waves of signals. The nymph’s only hope is to hold on until the mother arrives. But a thornbug is not built for speed, and the female moves slowly, like a tank over rough terrain. If she arrives in time, she gives the wasp a well-aimed kick, knocking it off the branch. After hovering for a few seconds, the wasp may fly off. Unfortunately for the thornbug family, however, the wasp is perfectly capable of remembering their location and is likely to return. And the next time, the wasp may manage, before the female arrives, to attack and bite a nymph’s legs, flip it onto its side, and roll off the stem with the nymph clutched in its front legs. The wasp then returns to its home colony, where, with the assistance of other workers, it chews its prey into smaller pieces to be fed to developing wasp larvae.
Whether or not she succeeds in protecting her young, the female makes her own distinct signals-a long series of rapid vibrational clucks-only after the wasp has left. As she clucks, the nymphs gradually quiet down. Following an attack, a group often changes shape, amoeba-like, as nymphs move to new positions, leaving some previously secure individuals exposed on the vulnerable edges of the group.
The combination of signaling nymphs and vigilant mother thwarts three out of four attacks by predatory wasps at my San Luis field site. But as experiments have shown, communication is successful only if the nymphs pool their efforts: mothers will respond to recordings of a synchronized SOS but not uncoordinated signals.
Several puzzles remain. For instance, why does the mother wait for the predator to leave before signaling? Perhaps the signaling informs her young of her continued presence; nymphs have been known to disperse when the female disappears. Also to be determined are the mechanisms behind the thornbug’s impressive vocabulary.
The degree of sibling cooperation in the thornbug is remarkable, but I have recently documented cooperative behavior among the nymphs of other treehoppers as well. In Calloconophora pinguis, for example, a species I studied in Panama, the chestnut-and-white nymphs (which sport spines like television aerials on their heads) exchange cowlike moos to signal the presence of rich feeding sites on their host plant. In this species, unlike the sedentary thornbug, family groups periodically move to better feeding sites.
Even after years of studying thornbugs and other treehoppers (also see Cicadas of Michigan), I still find it entertaining to watch the face of someone hearing their sounds for the first time. Occupying unexpected corners of acoustic space, some of these sounds could be mistaken for the unearthly songs of unknown whales, while others are strange mixtures of falling tones and explosive percussion. A few evoke laughs. Treehoppers are just one insect family among many that use vibrational channels of communication. The world of plant-borne sounds is still so little explored that it would not be surprising to find an ordinary backyard vibrating with hundreds of sounds that have never been heard by humans.
Many insects use plant-borne vibrations to attract a mate. Commonly a female responds to a signaling male not by approaching him (as would, for example, a female frog choosing a singing male) but with a signal of her own, usually different from and less elaborate than that of the male. As the two duet, the male searches for her, using her signals as a guide.
First, though, he must interest a female. Randy Hunt, of Indiana University Southeast, has studied the sexual signals of Graminella nigrifrons, a small, yellowish brown leafhopper that feeds on a variety of grasses in the eastern United States. The male of this species vibrates its abdomen to produce a complex song that, according to Hunt, begins with a piglike snort and progresses to repeated drumming with a Latin rhythm. Only females that happen to be on the same plant can pick up the signal, however, and if the male gets no reply, he quickly flies to another plant and tries again. This “call and fly” strategy is probably typical of many species.
Once a female answers a male’s calls, the challenge of finding her begins. The southern green stinkbug (so named because of the foul-smelling scent it releases when disturbed) appears to have an interesting technique. Andrej Cokl and colleagues at the National Institute of Biology in Slovenia placed male and female stinkbugs on ivy, a plant with many small stems. When a male stinkbug searching for a female comes to a branching point, he positions himself so that one set of legs touches one stem and another set touches the other. This position may enable him to detect differences between the two stems (in terms of the arrival time and amplitude of the female’s signals) and thus to determine which direction will take him to her.
Some insects, including many of the katydids and crickets that fill the summer night with their familiar songs, use both airborne sounds and plant-borne vibrations to communicate. When advertising for a mate, the male tropical cone-headed katydid (Copiphora rhinoceros), studied by Glenn Morris, of the University of Toronto, alternates between high-pitched airborne chirps and plant-shaking tremulations of its entire body. If a female walks onto his plant (in this species, the female moves toward the male), he switches from public chirps to the more private tremulations, thereby avoiding detection both by competing males on nearby plants, who might otherwise interfere with his courtship, and by bats that home in on acoustic signals.
The delicately beautiful green lacewing, common in meadows and gardens and along forest edges, signals by tremulating its abdomen, producing a low-frequency purr that travels through the plant stem. Some species of lacewing are unusual in that the male and female signals are virtually identical. The songs of all species, however, are quite distinctive—a characteristic that Charles Henry and Marta Wells, of the University of Connecticut, have used to identify a number of previously unrecognized lacewing species.
The diversity of plant-borne sexual signals is especially well illustrated in stoneflies. These insects spend their larval stages in water, most often in rocky streambeds, where their need for cool, clean, highly oxygenated water makes them good indicators of stream quality. After a male stonefly metamorphoses into adult form (which takes place out of the water), it begins signaling, usually by tapping or rubbing its abdomen on a stem or leaf. Studying these simple percussive mechanisms in different stonefly species, Kenneth Stewart and colleagues at the University of North Texas have discovered a tremendous variety of precise, intensely rhythmic signals.