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THREE

Fleeing and Staying under Cover

A well-hidden insect will be safe from many, if not most, insect-eating predators. But since natural selection is inexorable, predators will inevitably evolve with the anatomical and behavioral specializations needed to find and capture even the most thoroughly concealed insects. For example, if you hear what sounds like the blows of an ax in a winter woodland, it may well be a pileated woodpecker, the largest of our surviving North American woodpeckers, using its powerful, chisel-like bill to chop out chips of wood the size of a child's hand as it works to get at the larva of a long-horned beetle hidden deep in the trunk of a tree. An insect burrowing in the soil, such as a wireworm or a white grub, may be found by a mole or the probing bill of a grackle or some other bird. Nevertheless, hiding—although not always successful—can be advantageous, and insects of all sorts, and other animals too, have adopted this strategy for survival.

Natural selection favors—often very much so—an insect's normal lifestyle, especially its feeding behavior, if it keeps the insect out of sight and thereby protected from at least some potential predators. Usually only the larvae, insects in the immature stage, bore into plant tissues, burrow in the soil, or are otherwise hidden, and the usually immobile pupae generally remain hidden in the larval tunnel or burrow. The much more active adults are exposed to many more predators—spiders, insects, birds, mice, shrews, bats—as they fly and run about searching for nectar or other food, for a mate, and for appropriate places to lay their eggs. Most female insects lay hundreds of eggs, and many are exposed to predators as they fly long distances to distribute their eggs one by one or in small clutches on widely dispersed plants, often of only one or a few closely related species.

Figure 3. Disturbed by a predator, a grasshopper leaps into the air and flies off to make its escape.

In July and August we hear, high in the trees, the loud, shrill drone, the “love call,” of male dog-day cicadas—even in cities and towns. The females are frequently on the move as they disperse their eggs in small clutches laid in small cavities slashed into woody twigs by their sharp ovipositors, their egg-laying appendages. After hatching, the tiny nymphs drop to the ground and burrow deep into the soil, where they suck sap from roots until they emerge from the soil as adults about 2 inches long two or more years later. (Because the generations overlap, some cicadas emerge every year.)

Although the nymphs are relatively safe in the soil, the adults are eaten by birds of many kinds. Large, scary-looking but harmless solitary (nonsocial) wasps called cicada killers also search for them in the trees. The wasps inject them with a paralyzing but nonlethal venom, stock each of several small chambers in their underground nests with two or three of them, and lay a single egg in each chamber. (All but a very few nonparasitic wasps feed their larvae insect or spider prey.) The wasp larvae feed on the paralyzed cicadas but remain in the ground—as safely hidden from predators as are cicada nymphs—until they emerge from the soil as adult cicada killers the following summer.

Like the cicada killers, thousands of species of solitary wasps and bees prepare a shelter for their offspring. Most, like cicada killer larvae, live in burrows in the soil, but other parents build aboveground structures that shelter their offspring. (The Nobel laureate Karl von Frisch nicely described and illustrated some of these shelters in Animal Architecture) Some potter wasps (family Eumenidae), for example, build juglike nests of mud that they stock with paralyzed caterpillars, but other wasps of this family are not potters at all and instead nest in hollow plant stems.

Other insects also prepare concealed nurseries to hide their offspring from predators. Carpenter bees (subfamily Xylocopinae), some of which look like large bumblebees, excavate nesting tunnels as much as a foot long in solid wood—on one occasion in the unpainted cedar siding on my house, although they soon gave up because the inch-thick siding was too thin for them. Little brown solitary bees (family Andrenidae) hurry from blossom to blossom in early spring, gathering nectar and pollen from spring beauties. They dig long tunnels in the soil and provision small cells that branch off from the main tunnel with their harvest, which feeds the larvae that hatch from single eggs laid in separate cells. A remarkable mason bee (Osmia bicolor) of Europe prepares an individual nest for each of her larvae in the empty shells of land snails, perhaps even those that housed that gourmet's delight the escargot. After finding a shell, stocking it with food, on which she lays only one egg, and blocking the shell's opening, the bee, Frisch explained, “makes a series of flights to collect all kinds of dry stalks, blades of grass, thin twiglets, or even pine needles[;]…from this material, she builds a tentshaped roof over the snail shell, which eventually hides it completely.” Like all bees, both solitary and social, she provides her larval offspring with bee bread, a mixture of pollen and honey.

Their activities, seeking mates or places to lay their eggs, make it difficult or impossible for adults to always be hidden. Adult Japanese beetles, June beetles, and other herbivorous relatives of the scarabs feed on the foliage of shrubs and trees. Groups of metallic green and bronze Japanese beetles cluster shoulder to shoulder in conspicuous groups on a leaf. But both of these beetles and related species lay their eggs deep in the soil, including under our lawns. The chubby, C-shaped larvae, known as white grubs, live belowground, feeding on roots. Although well hidden and plagued by far fewer predators than the adults, they are preyed upon by some insects, birds, and moles. Among these predators are wasps of the family Scoliidae, which have no common name. John Henry Comstock noted that these wasps “do not exhibit as much intelligence as do most digger wasps; for they do not build nests and do not transport prey to them for their carnivorous larvae.” After locating a white grub in the soil, the female scoliid paralyzes it with a sting, “work[s] out a crude cell about it, and attaches an egg to…the grub.” The scoliid larva eats the grub, spins a cocoon, and completes its development in its underground cell.

Some immature insects hide in plant matter. The tiny leaf-mining larvae of some beetles, moths, flies, and wasps tunnel in the narrow space between the upper and lower epidermal layers of a leaf, feeding as they go. Their tunnels are clearly visible beneath the translucent epidermis. The tiny apple leaf miner moths glue their eggs to the undersides of leaves. When the larvae hatch, they pass through the egg shell directly into the leaf. Many beetle larvae and moth caterpillars, such as European corn borers, tunnel in the stems of nonwoody plants. Some snout beetles (weevils) gnaw a tunnel into an acorn or other nut with the mandibles at the end of their long, thin snouts and then turn around to place an egg in the tunnel and then move on to lay more eggs. When the full-grown larva emerges from the fallen acorn, it burrows into the soil to pupate. Some fly larvae, such as the apple maggot, and caterpillars, such as codling moth larvae—the infamous worm in the apple—burrow in fleshy fruits, but fly maggots leave the fruit to pupate in the soil, and codling moth caterpillars move away to pupate in a cocoon, often under a flake of bark on a tree trunk.

The sloth moths have what may be the most unusual lifestyle of all the insects, one that keeps them hidden from most, perhaps all, predators throughout the egg, larval, and pupal stages and exposes them only briefly during the adult stage. As adults, the four species of sloth moths, distant relatives of the European corn borer (family Pyralidae), hide in the dense growth of hair on sloths, slow-moving mammals of New World tropical forests that live high in the trees, feeding on foliage. Anywhere from a few to more than a hundred of these little moths may occupy a single sloth.

When sloth moths were first discovered in the nineteenth century, it was supposed that both the adults and the caterpillars lived on sloths and that the caterpillars fed on the plentiful growth of green algae on the sloths' hair or ate the hair itself. But in 1976 Jeffrey Waage and G. Gene Montgomery reported that although they found many adult moths on sloths, they found no eggs, caterpillars, or pupae. But they did find caterpillars feeding on sloth dung. About once a week a sloth descends to the ground to defecate. Hanging from a vine, it scoops out a pit with the long, curved claws on its hind legs, deposits about a cupful of fecal pellets in the pit, and covers it with leaf litter. Female moths briefly leave the sloth to lay their eggs on its yet-to-be-covered dung. The caterpillars eat dung, and when the moths emerge from the pupae in the dung pit, they fly up into the trees to find a sloth. They mate on the sloth, and gravid females leave the animal only long enough to lay their eggs.

Some insects construct their own hiding places. Working together, several hundred newly hatched tent caterpillars (Malacosoma americanum) of eastern North America spin a small tent of silk. As the caterpillars grow, they continuously enlarge the tent until it is about 2 feet long. Shaped like upside-down pyramids in the crotches of wild cherry trees, these tents are a common sight along country roads in spring. At night and during the cool parts of the day—early morning and late afternoon—the caterpillars shelter in the tent, where they are protected from many parasites and predators, Terrence Fitzgerald explained in The Tent Caterpillars. When it is warm enough, they leave the tent en masse and march nose to tail in single file to a leafy branch to feed, laying down a pheromone trail that will later guide them back to the nest.

Groups of other insects, mainly caterpillars, also cooperate to spin the communal silken nests in which they live. The messy nests of the fall webworm (Hyphantria cunea), constructed on the leafy branches of many kinds of trees, are a common sight in late summer in much of southern Canada and the United States. In spring and early summer, the webworm moths emerge from silken cocoons hidden under leaf litter or a flake of bark and lay their eggs in clusters of several hundred on the undersides of leaves. Upon hatching, the caterpillars immediately begin, as Ephraim Felt explained, “to spin a communal web under which they feed. This protecting web is extended to include more and more foliage till finally a considerable portion of a branch may be enclosed.” The caterpillars partly skeletonize leaves, eating only the upper surface, leaving the veins and the lower surface intact. “The skeletonized leaves within the nest soon dry, turn brown, and they, with the frass [excrement] and cast skins of the caterpillars, render the nests very unsightly objects.”

The caterpillars known as bagworms (family Psychidae) are well named. They live in cocoonlike pouches that they make of silk and decorate with bits of leaves and twigs. The head and thorax can be protruded through an opening in the bag, enabling the caterpillar to crawl and eat leaves. Fecal pellets are expelled through an opening at the other end of the bag. The familiar evergreen bagworm (Thyridopteryx ephemeraeformis) feeds mainly on junipers (red cedars) and arborvitae and, like other species of its family, spends virtually its entire life in its bag. The eggs laid by the wingless females overwinter in the bag. In spring, the newly hatched larvae leave the bag and immediately build their own bags, which they continually enlarge as they grow. In autumn, the fullgrown caterpillars pupate in their bags. The winged males emerge from the bags but, having vestigial mouthparts and unable to feed, live for only about a day. Drawn by a female's sex-attractant pheromone, a male thrusts his extensible abdomen far up into her bag and inseminates her. Only after laying their eggs do the larvalike adult females—which lack antennae, legs, and wings—emerge from the pupal skin, drop out of the bag, and die.

A cocoon protects many insects, most famously moths, during the pupal stage, when they are especially vulnerable to predators because being virtually immobile, they cannot run away or defend themselves. Before molting to the pupal stage, Comstock noted, caterpillars “make provision for this helpless period by spinning a silken armor about their bodies.” As we will see in chapter 9, several of the giant silkworm moths (family Saturniidae) of North America spin very large tough-walled cocoons, in which they spend the winter in the pupal stage. The huge cecropia caterpillar, for example, constructs a double-walled cocoon 3 or more inches long and immovably attached along its length to a sturdy twig.

In 1978, one of the two homes of the Green Revolution, the International Rice Research Institute (IRRI) on the island of Luzon in the Philippines, invited me to visit and develop a method for testing many thousands of rice varieties for resistance to the rice leaf folder, a moth of the family Pyralidae and an important rice pest. The main problem was figuring out a way to raise large numbers of leaf folder caterpillars in the laboratory so that the varietal tests could be done in a greenhouse. If the varieties to be tested are planted outdoors, the results of the test may be inconclusive, because as luck is likely to have it, the natural population of leaf folders will be too small or almost nonexistent that year.

Gottfried Fraenkel, who years before had supervised my PhD research, was invited to do the very same thing with rice leaf folders by the Central Agriculture Research Institute of Sri Lanka. About six months after I arrived at IRRI, Gottfried stopped off to see me on his way to Sri Lanka. When he asked me if I had made any progress, I oneupped my former boss, handing him a copy of a manuscript ready for publication that described my then recently devised method for testing rice plants for resistance to the leaf folder.

In Sri Lanka, Gottfried did other research projects with this insect, including a masterly study published in a Dutch journal in which he and Faheema Fallil wrote of the leaf folder, “Its characteristic behaviour is to spin a rice leaf longitudinally into a roll, by stitching together opposite rims of the leaf, and to feed inside this roll, leaving the epidermis on the outside of the roll intact,” as camouflage. Lying aligned with the long axis of the long, narrow leaf, the caterpillar swings the head end of its body from side to side in the same spot as many as one hundred times, forming a thick band of silk fibers that joins the edges of the leaf together. By repeating this procedure as it advances short distances along the leaf, the caterpillar forms as many as thirty such crossbands. “A newly woven band,” Fraenkel and Fallil found, “quickly becomes shorter by a process of contraction…bringing the rims of the leaf blade closer together…. With each succeeding band, this distance becomes shorter until the leaf is completely rolled up.”

If an insect's lifestyle does not commit it to living under cover, in hiding—or if it lacks an effective physical or chemical defense—it will most likely have another way of protecting itself against predators. Some insects, as we will see in chapters 4 and 5, are camouflaged, blend in with the background, or resemble an inedible object, but generally speaking, most defenseless species flee to a hiding place when they feel threatened—even camouflaged individuals whose cover is blown.

In 2008, Oswald Schmitz reported that red-legged grasshoppers (Melanoplus femurrubrum) respond differently to ambushing “sit and wait” spiders and to “roaming, actively hunting” spiders. Grasshoppers respond to sit and wait spiders, but not to roaming spiders, by shifting from their preferred food plant, a nutritious grass, to goldenrod, which is not a favorite food but on which they are less likely to be killed by a spider.

Most cockroaches, as Thomas Eisner and his coauthors so aptly put it, “crave concealment. Anyone who has shared a kitchen with cockroaches knows that they seek shelter by day and that they are driven to flee for cover at night if a light is turned on.” This is the way of not only the tiny minority of cockroaches that have become household pests but also most of the world's almost four thousand other cockroach species, which live in natural settings.

An insect that hides in a crevice or under a fallen leaf, a flake of bark, a rock, or a clod of soil would, ideally, have eyes not only on its head but also on its tail end so that it could tell if all of its body was safely tucked away in the dark of its hiding place. No insect or other arthropod has eyes on its tail end, but according to M. S. Bruno and D. Kennedy, a crayfish, a spiny lobster, and a shrimp have what Sir Vincent Wigglesworth called a “dermal light sense” at the tail end of the abdomen; in other words, in the “skin,” or exoskeleton (chitinous body wall). Actually it is not the skin but some part of the nervous system below it that can sense light. The American cockroach, and probably other cockroaches and many other insects, Harold Ball reported, has a similar light sensor at the tail end of the abdomen. There, a ganglion—a bundle of nerve cells and a part of the ventral nerve cord, which is, roughly speaking, the equivalent of our spinal cord—perceives light that passes through the translucent skin above it. Ball and other researchers demonstrated the existence of a dermal light sense. The American cockroach and other insects can tell light from dark even if the eyes on their heads have been covered with black paint.

Some insects, like cockroaches, rush to a hiding place if sufficiently alarmed. Others, such as the houseflies you startle in your kitchen, fly away rapidly but alight in plain sight on another wall. In either case, the fleeing insect was probably well served by an early warning system. “For species that are palatable,” Malcolm Edmunds pointed out, “it will be of advantage if they can detect their predators before the predators detect them, and if they can initiate their active defence (flight) before, or as soon as possible after, the predator has noticed them.”

Early warnings may be perceived by the organs of touch, vision, or hearing. At the tail end of the abdomen, noted R. F. Chapman, insects with gradual metamorphosis, except the true bugs, bear a pair of antenna-like sensory appendages, tactile receptors called cerci. Each cercus is clothed with fine hairs ultrasensitive to air currents or touch. This is, of course, an early warning system that alerts the insect to the approach from behind of something that might be a threat. Kenneth Roeder, an entomologist and neurophysiologist, described how the early warning signal of the cerci can be triggered. He suggested that “at night when cockroaches are most active, the observer should slowly approach a single insect standing motionless near the center of an unobstructed area such as a wall or floor. A short puff of air directed at the cerci…will send the roach scurrying off and probably out of sight.”

The early warning signal, a nerve impulse, travels along the insect's ventral nerve cord from the cerci to the ganglion in the thorax that controls the legs and launches the insect on its escape to safety. The faster the warning signal travels, the better. Among the many nerve fibers that constitute the ventral nerve cord of some insects, including the cockroach, are six to eight giant fibers as much as fourteen times as thick as the others. The virtue of the giant fibers is that they conduct nerve impulses much more rapidly, according to Roeder, at a rate of close to 23 feet per second rather than the other fibers' rate of no more than 2 feet per second.

Their ability to perceive distant objects often makes the eyes the most effective of the early warning systems. Most adult and nymphal insects have two compound eyes on the head, and many also have simple eyes (ocelli) between the compound eyes. Larvae have only simple eyes. The unusual structure of an insect's compound eye—radically different from that of our eyes or those of other vertebrates—gives it an exceptional ability to sense movements. A compound eye is an aggregation of closely packed but separate light-sensitive elements. “The system of small units…which constitute the compound eye,” Chapman explained, “lends itself to the perception of changes in stimulation resulting from small movements of [an] object.” This translates into a highly sensitive early warning system. For example, if you've ever tried to snatch a sitting fly, you know that it will, unless you are very fast, dash away long before your hand can reach it.

Except in the case of certain singing insects, Robert and Janice Matthews observed, “one does not usually think of insects as possessing ears.” Male singing insects—cicadas, crickets, and katydids are among the most familiar—belt out “love songs” to attract a mate. Females obviously must have ears, but males have them too, so they can listen for competing males. Most insects that don't make sounds do not have ears. But some mute insects of several unrelated groups—moths, lacewings, praying mantises—do have ears. If they are not listening to each other, what are they listening to? The answer, Roeder demonstrated, is fierce predators: night-flying, insect-eating bats.

In chapter 2 we saw that bats find their way in the dark by means of echolocation, a discovery made by Donald Griffin. They sense obstacles and flying insects by using their keen sense of hearing—many have very large ears—to listen for the echoes of their own sounds, pitched too high for us to hear, that bounce back from these objects. Flying insects that hear bat cries, Roeder found, respond by taking evasive action, which differs with the species: power-diving, folding the wings and falling to the ground, changing course, flying faster and more erratically.

An insect may flee from a predator by running, jumping, swimming, or flying, but many, notably plant feeders, just drop to the ground. With few exceptions, the insect is most likely to survive if it drops as soon as possible. The shaking of the branches and leaves of a tree or shrub may signal the arrival of a predator, most likely a bird hopping from twig to twig as it scans the foliage for insects. In response to a disturbance of this sort, some insects immediately bail out by dropping to the ground, a disappearing act that may happen even before the bird notices the insect. Some insects, notably aphids, disturbed by a bird—or more likely a ladybird beetle or an aphid lion—may simply drop from the plant. But, as Malcolm Edmunds notes, “few aphids respond to a predator by dropping, [although] this is always a successful method of escape. One disadvantage of dropping is that the animal may have great difficulty in finding and climbing a suitable plant on which to feed, particularly if it is immature and has no wings.” This is not a problem for leaf-feeding caterpillars of many species—and some spiders—which lower themselves more carefully and may climb back up on a thin strand of silk.

Some beetles, particularly snout beetles, respond to a disturbance by tucking in their legs and letting themselves tumble to the ground, where they are likely to lie motionless for some time. Many, as seen in the beautiful color photographs in Stephen Marshall's encyclopedic Insects: Their Natural History and Diversity, look deceptively like dark fecal pellets or small clods of earth. Among the latter group is the well-disguised quarter-inch-long plum curculio (Conotrachelus nenuphar), which is brown with a few small white markings and four large humps on its back (wing covers). Fruit growers take advantage of these insects' escape behavior to find out if they are numerous enough in plum, peach, or apple orchards to justify the expense of an insecticide application. “Jarring the beetles from the trees in the early morning, on sheets placed on the ground,” explained Robert L. Metcalf and Robert A. Metcalf, “enables the grower to…[census the population] of these beetles.”

The forked fungus beetles (Bolitotherus), named for a pair of prominent “horns” that protrude from just behind the male's head, have an escape behavior similar to but even more impressive than the plum curculio's. Adults and larvae of this eastern North American species feed on the shelf, or bracket, fungi commonly seen protruding from the trunks of dead trees. If they are disturbed, Marshall observed, the adults' “first defensive response is to pull in their appendages and drop to the ground.” Legs and antennae protectively retract into special grooves. The beetles don't move, “feigning death,” and are difficult to spot because they look even more like clods of earth than the plum curculio. In addition, adult forked fungus beetles have a chemical defense, an irritating substance secreted by an eversible forked gland at the tip of the abdomen. But the most amazing thing about these beetles is their early warning system, described by Jeffrey Conner and his coworkers. The beetles recognize “mammalian breath on the basis of its temperature, moisture, and flow dynamics,” which causes them to evert the gland, but they do not respond to a mechanically produced air stream. The beetle's “ability to cue in on mammalian breath enables it to respond preemptively to a potentially lethal attack from a ground-foraging mammal, perhaps a deer mouse. Gland eversion can save the beetle by making it distasteful at the very moment that it is taken into the predator's mouth, before a bite is inflicted.”

Many insects, especially ground-dwelling species such as cockroaches and beetles, run away as rapidly as they can when alerted by their early warning system. There are, however, surprisingly few records of how fast they can go. My friend and colleague Fred Delcomyn, a neurophysiologist and an expert on the neural control of walking and running by insects, told me that it is very difficult to time running insects because they rarely go very far in a straight line. The American cockroach, according to G. M. Hughes and P.J. Mill, is one of the fastest insects, running at a maximum speed of 51 inches per second, or 2.9 miles per hour. This may seem slow, but consider the rate compared to body length. The American cockroach runs a distance of about thirtyfour times its body length of 1.5 inches in one second. This is equivalent to a coyote with a body length (excluding the tail) of 2.8 feet running 65 miles per hour. I doubt coyotes can run that fast. (I once clocked a panicked one going 45 miles per hour trying to outdistance my pursuing car as it ran along a ditch bank parallel to the road I was driving on.) It seems, then, that on the basis of a fair comparison, the American cockroach is probably a faster runner than a panicked coyote. Keep in mind that some of the thousands of cockroach species that live outdoors—and surely have many enemies other than irate householders—run at least as fast as and perhaps even faster than the pestiferous American cockroach.

A sudden leap into the air is another good way to escape from a predator. It is not surprising, then, that many different kinds of insects, members of several unrelated groups, have evolved this escape tactic independently of one another—and have jumping apparatuses fashioned in quite different ways, and even from different body structures. Grasshoppers, crickets, and katydids are closely related and probably inherited their jumping hind legs from a common ancestor. But fleas, flea beetles, and certain relatives of the aphids and cicadas, such as leafhoppers and planthoppers, have leaping hind legs that obviously evolved independently of each other and may be quite different in design. Click beetles and springtails, close relatives of the insects that I discuss below, leap into the air without using their legs.