Читать книгу How Not to Be Eaten - Dr. Gilbert Waldbauer - Страница 9
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The Eaters of Insects
In the middle of the night, a little bolas spider hangs from a plant by a few threads of silk. When a flying moth comes close enough, the hungry spider flicks at it a length of silk thread with a droplet of very sticky glue at the end. This is its bolas. With a bit of luck, the glue catches the moth, which the spider reels in and makes a meal of. The bolas spider's weapon is unique among animals—except for humans, who have invented similar weapons, the lasso and the Argentine gaucho's bolas, for which the spider is named. The spider doesn't just wait for an insect to wander along. It lures in its prey, which are always moths, by means of a false signal, a counterfeit version of the odorous sex-attractant pheromone released by the female moth to attract a mate. The clue that led to the discovery of this surprising chemical subterfuge is that these spiders catch only male moths of one species.
The bolas spider is just one among hundreds of thousands of animals that eat insects and is by no means the only one that has evolved an ingenious way of capturing its prey. The most abundant of the insectivores are themselves insects, at least three hundred thousand species. The other insectivores are far fewer, but they run the gamut of the animal kingdom: spiders, scorpions, centipedes, fish, frogs, toads, salamanders, turtles, young alligators, lizards, snakes, birds such as woodpeckers, nuthatches, swifts, swallows, and warblers, and mammals such as anteaters, armadillos, skunks, shrews, mice, bats, and even bears.
Figure 2. A pair of burrowing owls have placed clumps of cow manure around the entrance to their burrow, a bait that attracts dung beetles, which the owls will eat.
The eaters of insects have evolved innumerable tactics and strategies for finding, capturing, and consuming their share of this great multitude of creatures. Dragonflies course over ponds, capturing mosquitoes in a basket formed by their spiny legs. Well-camouflaged praying mantises sit motionless as they patiently wait to grab passing insects with their raptorial front legs. Among the birds, colorful warblers flit from twig to twig, rapidly scanning leaves for caterpillars; flycatchers dart from their perches to snap up flying insects; and blue jays sometimes scan tree trunks for camouflaged moths that blend in with the bark on which they rest during the day. Bats employ sonar—echolocation—to find flying insects at night. An armadillo uses its long, sticky tongue to capture the ants, beetles, and other insects it uncovers as its rather long snout furrows through leaf litter and loose soil. We usually think of squirrels as vegetarians, but William Burt watched a thirteen-lined ground squirrel dig in the soil for white grubs (the larvae of a June beetle). The bolas spider's tactics are unique, but other spiders use a variety of quite different hunting strategies. Among them are spiders that spin the familiar webs of sticky silk that snare flying insects, wolf spiders that chase their prey, and spiders that lurk in tunnels covered by trapdoors and dash out to grab and envenom passing insects that stumble into their trip wire, a single strand of silk.
The familiar flat, circular webs spun by the orb-weaving spiders are sticky lacework nets designed to catch unwary insects that blunder into them. Although they are marvels of engineering, they are also very beautiful, poems in symmetry—especially in early morning, when they glitter with little drops of dew. Long, straight strands of silk, which are not sticky, radiate from the hub of the web like the spokes of a wheel. Interspersed among them are long strands of exceedingly sticky silk that form a sequence of closely spaced loops spiraling from the hub of the web to its outer edge.
When the spider, waiting motionless on the hub, feels the vibrations caused by a struggling insect stuck to the web, it plucks the radial threads one by one, “apparently,” wrote Rainer Foelix, an expert on spider biology, “to probe the load on each radius. In other words, it tries to find the exact position of the prey.” It then “will rush out of the hub using exactly that [nonsticky] radial thread which leads to the prey.” Only after it has wrapped the prey in silk does it administer its venomous bite. The spider “then cuts the neatly wrapped ‘package’ from the web and carries it to the hub. There it is attached by a short thread before it is eaten.”
Few insects other than moths, as Thomas Eisner and his coworkers discovered, manage to escape from the webs of orb-weaving spiders. Moths are sometimes saved by the tiny, easily detached scales that cover their wings and bodies. (The colored “powder” that clings to your fingers when you handle a moth or a butterfly consists of these scales.) Moths that blundered into a web, Eisner noted, “were detained only momentarily, and usually flew off seemingly unaffected by the encounter. However, they invariably left behind, stuck to the particular viscid threads…that bore the impact, some of the scales that ordinarily cover their wings and bodies…. Coated with scales, the threads are no longer adhesive, and the moth is free to escape.”
On a sunny June day in northern Michigan, I spotted an interesting-looking insect on a large white blossom of a Canada anemone. (It turned out to be a fly that mimics a yellow jacket wasp. You will read a lot more about mimicry in later chapters.) This insect, oddly enough, wasn't moving at all, and its posture seemed unnatural. Looking more closely, I saw that it was clutched by a white crab spider that was all but invisible on the flower. Many crab spiders, like this one, are ambushers that lurk motionless in a blossom as they wait for their prey to land—a fly, bee, or other insect. Some can, in the course of about a week, change from white to yellow or yellow to white to match the color of the blossom on which they are lurking. “Fortified with extremely potent venom in compensation for weak Chelicerae [pincers], the small crab spiders,” Foelix commented, “are formidable creatures that attack insects and other spiders much larger than themselves.”
The fact that these spiders evolved the ability to change their color suggests that at least some insects are wary and will not land on a flower occupied by something that might be a predator. In The World of Spiders, W. S. Bristowe described a simple experiment which showed that this seems to be so. On half of sixteen yellow dandelion blossoms that he had placed on a lawn, he put a black pebble about the size of a crab spider; on the other half he placed a pebble that was about the same size but matched the dandelion blossom's color. As Bristowe watched these blossoms for half an hour, only seven insects visited the ones with black pebbles, while fifty-six flies and bees visited the blossoms with yellow pebbles.
Some insects, such as the familiar praying mantis, are predators that, like a tiger or a wolf, during their lives will capture many prey animals and more or less immediately kill and eat them. Other insects, mainly many of the wasps and all of the flies of the family Tachinidae, according to Richard Askew, are parasites that develop from egg to full-grown larva within the body of just one host, usually an immature insect—perhaps a beetle grub, a caterpillar, or a grasshopper. However, parasitic insects are best referred to as parasitoids. True parasites, such as the intestinal worms of humans and other mammals, usually do not kill their hosts. But although a parasitoid begins relatively benignly, just absorbing nutrients from its host's blood, it eventually becomes a predator, killing its host by devouring its tissues.
Among the many thousands of insects that parasitize other insects, the wasps of the genus Trichogramma (they have no common name) are particularly interesting because of their habits and because agriculturalists disperse them in fields to protect various crops from leaf-eating caterpillars. These tiny wasps—the largest are only about 0.04 inches long—insert their eggs into the eggs of many different kinds of moths and butterflies. The Trichogramma larvae destroy the host egg by consuming its contents. The size and even the anatomy of the adult parasite that emerges from the egg, Askew explained, varies with the size and species of the host egg. Wasps reared from the large eggs of a cutworm moth were nearly twice the size of those of the same species reared from the much smaller eggs of a grain-feeding moth. Males of another species reared from a moth egg had normal wings, but those reared from an alderfly egg had no wings at all. Trichogramma wasps can be raised by the millions in the eggs of a domesticated colony of grain moths. If a crop, perhaps cotton, is likely to be seriously damaged by the caterpillar progeny of egg-laying moths, Trichogramma are often released in the field in the form of larvae developing in grain moth eggs that had been glued to slips of paper by their mothers.
Many nonparasitic insects that feed on other insects are hunters that actively pursue their prey. Robber flies (family Asilidae) dart from a perch, perhaps the tip of a twig on a low shrub, to snatch flying insects from the air. When the fly comes back to land, it sucks its victim dry after injecting it with a secretion containing poisons that kill it and enzymes that liquefy its inner tissues. Almost all of the more than 2,600 species of ground beetles in North America are insectivores, such as the colorful, inch-long, tree-climbing caterpillar hunters (genus Calosoma). Adult cicada killers (Sphecius speciosis)—wasps barred with yellow and black and about 1.5 inches long—are vegetarians that sip nectar from flowers but search trees for the dog-day cicadas that they will feed to their larvae ensconced in underground cells.
Ambushers, by contrast, are stealthy insects that are generally well camouflaged and sit motionless as they wait patiently for their prey to come along. Like the white crab spider, ambush bugs (family Reduviidae) lurk on flowers, often goldenrods, waiting to snatch up with their raptorial front legs a visiting nectar feeder, such as a bee, a wasp, or a butterfly. As do all of the other true bugs, they have piercing-sucking mouthparts, which the nonvegetarians use to suck their prey dry, rather than masticate it like the mantises and other insects with chewing mouthparts.
One of the most deceptive of the ambushing insects is a southeast Asian praying mantis (Hymenopus bicornis) that masquerades as a pink flower of the straits rhododendron, a shrub known as the Sendudok in the Malay language. Hugh Cott summarized Nelson Annandale's 1900 account of the appearance and behavior of this remarkable insectivore in the report of the University of Cambridge's expedition to the Malay Peninsula. The bright pink mantis, the color of the blossoms among which it rests, is patient and motionless as it waits for its next meal to come close enough to be snatched. Its deception is enhanced by wide pink petal-like flanges on its middle and hind legs. Insects, as Wolfgang Wickler noted, actually land on the mantis's body and probe for nectar, “for which they pay with their lives.” Its “alluring colouration,” as Hugh Cott put it, is a bait that attracts the insects that it eats. This is one of many examples of aggressive mimicry, the duping of potential victims, causing them to relax their guard. The mantis's disguise may also save its life. Insectivores such as lizards and birds are likely to pass it up because it is so deceptively camouflaged.
The mantis's ruse is most effective when it lurks among blossoms that it resembles. Consider Nelson Annandale's account of the dogged persistence of one such insect as it searched for an appropriate resting place. A captive mantis put on the ground near a large branch of a Sendudok
deliberately walked towards the branch, swaying its whole body from side to side as it progressed, and commenced to climb one of the twigs. This twig, however, bore only green buds and unripe fruit. When the Mantis reached the tip of the twig and found no flowers, it remained still for a few seconds, and then turned and descended with the same staggering gait. It proceeded to climb another twig. This also bore no flowers. The Mantis descended from it and mounted a third twig which was topped by a large bunch of full-blown blossoms. To these it clung by means of the claws of the two posterior pairs of limbs. For a few minutes it remained perfectly still, and then began swaying its body from side to side, as it had done while walking.
Annandale, quoted by Cott, tells us how well this mantis's aggressive mimicry deceives the insects that it will eat.
Almost as soon as the Mantis had settled itself on the inflorescence, a small, dark…[fly] of a kind very commonly seen on the flowers of this species of [shrub] alighted on one of its hinder legs. It was soon joined by others, apparently of the same species as itself. They settled quite indiscriminately on the petals and on the body and limbs of the Mantis…. The Mantis made no attempt either to drive off or to capture the small flies, for its motions seemed to attract rather than to repel them. After a short time a larger [fly,] as big as a common house-fly, alighted on the inflorescence within reach of the predatory limbs. Then the Mantis became active immediately; the fly was seized, torn in pieces and devoured, notwithstanding the presence of a large crowd of natives who had collected to watch what was happening.
This form of mimicry is not confined to insects, as we have seen. Even plants take advantage of insects, such as orchid blossoms that mimic female wasps or bees and are pollinated by soon-to-be-disappointed males that try to copulate with them. Wickler also described a particularly interesting and illuminating aggressive mimicry in a marine environment. Small fish known as cleaners stake out territories on coral reefs. Other fish know where to find them and have learned to recognize them by their distinctive appearance and the little “dance” they do to attract customers. Just as we visit our barbers and hairdressers, various kinds of fish show up regularly for a thorough delousing. Customers let the cleaner search their body—even their gills and the inside of the mouth—for external parasites, which it removes and eats. A fish aptly named the saber-toothed blenny mimics the cleaner—even imitating its dance. If a fish looking for a cleaning is hoodwinked by the mimic, it gets a nasty surprise: the mimic takes a big, painful bite out of one of its fins. The startled victim wheels around, “but the mock cleaner calmly stays put as if knowing nothing about it, and remains unmolested because of its cleaner's costume,” as Wickler wrote.
A few caterpillars are aggressive mimics that eat other insects. Almost all of the world's 125,000 known species of moths and butterflies (order Lepidoptera) are vegetarians that munch on leaves or other plant parts in the caterpillar stage. Among those exceptions known for many decades are about fifty species that, as Walter Balduf reported, eat scale insects that are immovably attached to a plant or are virtually incapable of moving. Only about thirty years ago, Steven Montgomery made the amazing discovery that fifteen kinds of inchworms, caterpillars of the moth family Geometridae, are ambush predators that capture active, highly mobile insects—unique exceptions among the one thousand plant-feeding species of the worldwide genus Eupithecia. These inchworms exist only in Hawaii, where they evolved from a vegetarian ancestor that arrived on these isolated volcanic islands after they had arisen from the sea more than five million years ago. The various species, all suitably camouflaged, wait in ambush on different perches: green leaves or stems, brown twigs or fallen leaves. As other inchworms often do to make themselves inconspicuous, these ambushers use claspers at the posterior end of the abdomen to hold on to their perch, from which they stretch their bodies straight out, and freeze in position. On a twig they look like a short branching spur. “When a prey animal touches [its] posterior end,” Montgomery wrote, “the caterpillar suddenly loops backwards to seize the prey with its thoracic legs…and quickly returns to a straightened, elevated posture to feed. The entire strike takes about second.” The thoracic legs are elongated and “armed with enlarged spine-like setae and sharp claws.”
Unlike the many web-spinning spiders, only a few terrestrial insects fashion traps to catch their prey. But several years ago, Alain Dejean and his coworkers published an account of traps built by a tree-dwelling ant (Allomerus decemarticulatus) of French Guiana. As do quite a few other ants, Allomerus has a mutually beneficial association with a particular species of plant. The plant provides leaf pouches in which the ants nest, and the ants reciprocate by destroying insects that feed on the plant. Dejean and his coauthors reported that the ant “uses hair from the host plant's stem, which it cuts and binds together with purpose-grown fungal mycelium [long threadlike strands], to build a spongy ‘galleried’ platform for trapping much larger insects. Ants beneath the platform reach through…holes and immobilize the prey, which is then…transported and carved up by a swarm of nestmates.”
The most famous of the trap-making insects are the ant lions of the order Neuroptera, relatives of the aphid-eating green lacewings. Harold Bastin described how an ant lion larva digs its pitfall trap in the soil:
The larva is a strange-looking insect, thick-set and somewhat oval in contour, with a flat head armed with formidable, curved mandibles. It has an ingrained habit of walking backwards, and uses its convex abdomen as a plough. When constructing the pitfall for which it is famous, it usually begins by making a circular groove to correspond with the margin of the proposed excavation. It then ploughs round and round in diminishing circles, constantly jerking out the sand with its shovel-like head. The final result is a funnel-shaped hollow, in the bottom of which the maker lies buried with only its ugly jaws exposed to view. Any small insect which chances to run over the edge of the pit slides downward on the yielding sand, its descent being hastened by the ant-lion, which casts up jets of sand upon its victim.
After its fanglike mandibles inject the victim with venom and digestive enzymes that liquefy its internal tissues, the ant lion sucks up its predigested meal—much like a robber fly or an ambush bug.
It is a wonder of evolution that a fly (genus Vermileo) maggot, or larva, of the snipe fly family (Vermileonidae) has independently invented this trap. In Demons of the Dust, William Morton Wheeler described how this larva, the worm lion, digs its pitfall:
The procedure is very simple compared with the usual circuitous performance of the ant-lion, because the worm-lion merely curls its anterior end after thrusting it in the sand and then suddenly straightens it, thus tossing the sand out onto the surface. At the same time it rotates more or less on its long axis, so that the direction in which the sand is thrown differs somewhat with each discharge. In this manner a small conical pit, with the larva at its apex, is soon formed…when the pit is completed the larva awaits its prey…. Usually…it lies horizontally on its back with its posterior half buried in the sand and its thoracic and first abdominal segments crossing the floor of the pit like a bar and covered with a very thin layer of sand.
When an insect falls into the pit, the worm lion usually strikes “at the prey violently and repeatedly till it [can] fix its mandibles in some portion of its body.” Next “it pump[s] venom into its victim and then commence[s] imbibing its juices.”
The delightful robin-sized burrowing owls of the Great Plains and southern Florida are very unusual. Unlike most owls, they are partly diurnal, unusually long-legged, live and nest in burrows that they dig to a depth of as much as 8 feet, and spend much of the day surveying their surroundings from the top of the large mound of excavated soil. If alarmed, perhaps by a birdwatcher or an approaching predator, they give a loud chattering call as they agitatedly—and amusingly—bob and bow.
One of the more remarkable things about these little owls is that they scatter chunks of horse or cow dung (probably bison dung earlier in the species' history) around the entrances of their burrows. The dung is evidently important to them, because if it is removed, they will usually replace it. What purpose the dung serves was a mystery until Douglas Levy and his coworkers showed that it is bait to attract dung beetles, relatives of the scarabs, that the owls eat. The researchers' first step was to remove all dung, beetle scraps, and regurgitated owl pellets (which contain the indigestible parts of beetles and other prey) from around the entrances to twenty occupied burrows. Then they put a quantity of cow dung “typical of the amount [usually] found at a burrow entrance” around the entrances to half of these burrows and none around the entrances to the other half. After four days, they collected the dung beetle scraps and regurgitated pellets from around the entrances to all the burrows. Then they repeated the experiment, switching the bait from one group of burrows to the other. Examination of the beetle remains found on the ground and in the pellets showed that “when dung was present at the burrows, owls consumed ten times more individual dung beetles of six times as many species than when dung was not present.” The inescapable conclusion is that burrowing owls use dung as bait. The use of bait to catch insects is, indeed, very unusual for a bird, but not unique. On several occasions a green heron was seen catching fish attracted to bits of bread that it had dropped on the water at the edge of a pond in a park.
Birds have evolved many other truly remarkable anatomical, physiological, and behavioral adaptations for exploiting insects as food. Roger Tory Peterson's words put the birds and insects in an ecological context, neatly setting the stage for a look at birds as predators of insects:
The insects, which have invaded nearly every terrestrial environment on earth, are unable to evade the birds that probe the soil, turn over the leaf litter, search the bark, dig into the trunks of trees, scrutinize every twig and living leaf. The water is no safe refuge, nor is the air, nor the dark of night. There is a bird of some sort to hunt nearly every insect. Warblers and vireos methodically work the leaves while swallows, swifts and other hunters of flying-insect prey spend most of their waking hours on the wing, ranging hundreds of miles daily in their aerial forays.
This story began about 155 million years ago with the first known bird, the famous Archaeopteryx, represented by beautiful, complete fossils from a limestone quarry in Bavaria. Archaeopteryx combined avian and reptilian characteristics, which shows—as do more recently discovered feather-bearing dinosaur fossils from China—that the birds are direct descendants of the dinosaurs. During the next 120 million years many species of birds evolved, but relatively few of them were insect eaters. During the Miocene epoch, beginning about 30 million years ago, the rapid evolution of the flowering plants and the hundreds of thousands of insects that exploit them resulted, as Frank Gill noted, in an explosive evolutionary radiation of insectivorous birds, mainly songbirds (order Passeriformes), which today constitute close to six thousand of the almost ten thousand known species of birds.
Most birds include insects in their diet. With few exceptions, most notably pigeons and doves, even the most dedicated vegetarian birds, fruit and seed eaters such as finches, buntings, grosbeaks, and cardinals, feed their nestlings a high-protein diet of animal matter, mainly insects. The behavior of a cardinal observed by Josselyn van Tyne is illustrative: “At noon on May 24 the adult male, on his way back to the nest territory, stopped at my feeding shelf with his beak full of small green worms [caterpillars] such as I had often fed to the young. He immediately put the worms down on the shelf and began cracking and eating sunflower seeds…. He then picked up the worms, flew across the street, and (presumably) fed the young.”
Insect eaters avoid competition by sharing the environment, specializing in where and how they hunt. Ground feeders such as towhees and fox sparrows search the litter on the forest floor for both insects and seeds; warblers, chickadees, and other leaf gleaners search foliage for caterpillars and other insects; nuthatches and brown creepers are among the bark gleaners; wood and bark probers, such as woodpeckers, bore into trees to find grubs and other burrowing insects; flycatchers and, on occasion, many other birds are air salliers that dash from a perch to snatch insects from the air; and finally, gleaners of aerial plankton, among them swallows, swifts, and nightjars, more or less constantly swoop through the air to scoop up flying insects.
As Peterson elaborated, avian insectivores have become specialized to exploit insects as food in many different ways. Take, for example, the many birds that snatch flying insects on the wing. Most of the thirty or more flycatchers (family Tyrannidae) that nest in the United States and Canada wait quietly on a perch, often a bare branch with a clear view of the surrounding airspace, from which they dash out to snap up passing insects. They usually return to the same or a nearby perch to wait for another insect to fly by. One of the most familiar of the tyrant flycatchers is the eastern kingbird, often seen perched on fence wires along country roads. This gray and white bird, truly a pugnacious tyrant, attacks and chases away any birds that come too close to its territory, even crows, hawks, and vultures. From Nebraska south to Texas, the exquisitely beautiful pink and pearly gray scissor-tailed flycatcher, its forked tail twice as long as its body, is a “wire bird” that likes to perch on telephone lines along the roadside. The little brown tail-pumping eastern phoebe, which often builds its mud-based nest under a bridge or on a rafter in an outbuilding, is one of the first birds to return to the northeastern United States, as early as March. “Now and then,” Edward Forbush and John May wrote, “one of these early birds may be seen darting out from its perch in a March snowstorm, apparently catching insects.”
Tyrant flycatchers will eat almost anything that flies, as well as small caterpillars and spiders that “balloon” through the air on long strands of silk. Several species even eat wasps and bees, because they can avoid being stung or can recognize and catch only stingless males. Some beekeepers believe that the brown-crested flycatcher, which preys on bees in apiaries, is a pest that eats worker bees. A discerning Arizona beekeeper, quoted by Herbert Brandt in Arizona and Its Bird Life, at first agreed “but after examining the stomach contents of a large number of [brown-crested flycatchers] during a period of more than 20 years, and not in a single instance finding the remains of a worker bee, nor finding a bee sting in the mouth or throat of one of these birds, became convinced that [they] did not prey on worker bees, but only on drones [the stingless males].”
Many birds are opportunists that will flycatch when a flying insect comes temptingly close. I have seen warblers of several species put their search for caterpillars on hold as they darted out from a leafy branch to catch a passing fly. Even a nuthatch crawling on a tree trunk will stop searching for insects on the bark to pursue a flying insect. Cedar waxwings feed mostly on small fruits such as chokecherries and blackberries. But “in late summer and early fall,” Forbush and May noted, “the cedar waxwing turns to flycatching, and taking its post on some tall tree, usually near a pond or river, launches out over water or meadow in pursuit of flying insects.” Birds caught at such times have been found crammed to the very beak with insects.
The birds commonly called goatsuckers (order Caprimulgiformes, from the Latin roots for goat and milk) are seldom-seen night fliers that eat almost nothing but insects. (Their odd common name stems from the European myth that they suck milk from goats.) At night, the loud and clearly enunciated calls of most of the North American goatsuckers not only make their presence known, but tell us their common names, which are verbal renditions of their calls: whip-poor-will, poor-will, and chuck-will's-widow. The common nighthawk is an aberrant goatsucker that flies both at night and during the day and, unlike the others, is likely to live in a city, laying its well-camouflaged eggs not in a nest but on the surface of a flat, gravel-covered roof.
Goatsuckers have wide, gaping mouths with which they scoop insects from the air. Except on the nighthawk, stiff bristles surrounding the mouth expand the “scoop.” Goatsuckers eat night-flying insects of almost any kind; among others, mosquitoes, June beetles, flying ants, and moths, including even large moths with 4- to 5-inch wingspans, such as cecropia, luna, and polyphemus. Larger than the other goatsuckers at a length of almost a foot, the chuck-will's-widow occasionally eats small birds. The goatsuckers are the night shift of the birds that harvest the many night-flying insects and ballooning spiders that crowd the air. As we will soon see, they are joined by bats, which fly much higher than most of the goatsuckers.
The swifts, the swallows, and the nighthawks—the last working days only part-time—are the day shift of the birds that subsist on aerial plankton. There is little competition between them because nighthawks are seldom numerous and the swifts and the swallows, which are usually very numerous, have found a way to share the airspace. Swallows tend to hunt a relatively short distance above the ground, usually at a height of only a few yards. Swifts, on the other hand, fly much higher. Chimney swifts, the only members of their family in eastern North America, live in towns and cities and, almost constantly on the wing from sunrise to sunset, fly well above the tallest church steeples. Before the advent of Europeans in the New World, chimney swifts glued their twig nests to the inner walls of hollow trees. Today practically all of them prefer to nest in chimneys.
Several of the eight North American swallows have also become associated with humans. Most of us view the colorful, fork-tailed barn swallow, the most familiar of these birds, with affection. They usually nest inside a barn or other outbuilding, sticking their feather-lined mud nests to a wall or placing them on a rafter or some other support. An opportunistic hunter, a barn swallow takes advantage of every occurrence that makes insects easy pickings. Forbush and May wrote that “it follows the cattle afield or swoops about the house dog as he rushes through the tall grass, and gathers up the flying insects disturbed by his clumsy progress. When the mowing machine takes the field, there is a continual rush of flashing wings over the rattling cutter-bar just where the grass is tumbling to its fall. The Barn Swallow delights to follow everybody and everything that stirs up flying insects—even the rush and roar of that modern juggernaut, the motor-car, has no terrors for it.”
Other birds take advantage of similar opportunities. In spring I sometimes see flocks of ring-billed gulls in recently plowed central Illinois fields, harvesting soil-dwelling insects turned up by the plow, probably including fat cutworm caterpillars that would have become night-flying moths; C-shaped white grubs, the larval stage of June beetles; larval click beetles, the skinny, brown wireworms; perhaps the overwintering pupae of a corn earworm moth. In Africa, cattle egrets snatch insects flushed up by large grazing animals. We also see these birds associated with grazing cattle in southern Ontario and most of the continental United States. They were first seen on this side of the Atlantic in northern South America about one hundred years ago, a flock probably aided by the trade winds having crossed the ocean. In tropical America, ant birds (family Formicariidae) follow swarms of army ants, feeding on insects the ants flush up as they advance over the forest floor.
Birds that eat insects associated with trees, as we have seen, can be grouped into several quite different feeding guilds. These specializations are driven by competition between species, which forces birds to share the available insects. In 1934, G. F. Gause pointed out that “as a result of competition, two similar species scarcely ever occupy similar niches, but displace each other in such a manner that each takes possession of certain peculiar kinds of foods and modes of life in which it has an advantage over its competition.” This is the competitive exclusion principle.
“Species that coexist in seemingly homogeneous habitats, such as grasslands or spruce forests,” Frank Gill wrote, “may segregate their niches even more finely.” Five insectivorous wood warblers, colorful species that migrate back and forth from the New World tropics to where they nest in the spruce forests of the north, manage to coexist on the same spruce trees by feeding in different ways on particular parts of the trees, as Robert MacArthur discovered. Gill's concise summary of MacArthur's observations explains how the warblers avoid competing with one another: “The yellow-rumped warbler fed mostly in the understory below 3 meters [almost 10 feet], the black-throated green warbler in the middle story, and the blackburnian warbler at the tops of the same spruce trees. Sharing the middle part of the trees with the black-throated green warbler, which explored the foliage for food, was the Cape May warbler, which fed on insects attracted to sap on the tree trunk. Sharing the treetops with the blackburnian warbler, which fed on the outer twigs and sallied out after aerial insects, was the baybreasted warbler, which searched for insects close to the trunk.”
In addition to almost all of the fifty species of warblers that can be seen in the United States and Canada, other birds also make a living by searching foliage for insects. A few among the many are the vireos, orioles, tanagers, kinglets, titmice, and chickadees. The spry little black-capped chickadees are agile acrobats that nimbly hop from twig to twig and may hang upside-down as they inspect a leaf for their next meal, which is likely to be a caterpillar. They are particularly interesting because they display what—at least in my view—can only be called intelligence as they search for their prey. Their hunting behavior, Bernd Heinrich and Scott Collins found, is amazingly clever and sophisticated. As we will see in chapter 9, they keep an eye out for partially eaten leaves—those that are tattered or holey—which, they realize, indicate that caterpillars are probably nearby.
Some birds are preoccupied with the trunks and larger branches of trees: bark gleaners, such as the brown creeper and white-breasted nuthatch, and bark and wood probers, such as woodpeckers and, of all things, a very unusual finch on the Galápagos Islands. The brown creeper has an energy-efficient way of searching a tree trunk for insects, spiders, other small creatures, and their eggs tucked away in the crevices of the bark. It begins at the base of the trunk, which it climbs up in a spiral path while conducting its inspection. When it is ready to move on, it spreads its wings and, expending a minimum of energy, glides down to the base of a nearby tree trunk and begins another upward climb as it hunts for food. The white-breasted nuthatch frequently crawls headfirst down the tree trunk. From this perspective it is likely to find food that brown creepers miss. In winter, nuthatches supplement their diet with plant food, such as acorns and sunflower seeds, which they often conceal in bark crevices for future use, a behavior that inspired their common name.
The woodpeckers (twenty or more species in North America), Roger Peterson wrote, “spend most of their lives in a perpendicular stance, clamped against a trunk or a branch, the stiff tail acting as a brace and the deeply curved claws, two forward, two aft on each foot, clutching the rough bark. The straight beak, hard as a chisel, is driven in triphammer blows by powerful muscles in the head and neck.” The beak is used to find wood-boring insects by gouging into solid wood, and to excavate its own deep nesting cavities. Beetle grubs and other insects are extracted from their burrows by a barbed tongue that can extend as much as five times the length of the bill, a tongue so long that it can be stored in the head only by looping around the skull. A physician quoted by Steve Nadis wondered what makes it possible for these birds to use their head “as a battering ram without sustaining headaches, concussions or other brain injuries,” why dead and dying woodpeckers don't litter the countryside. Dissecting woodpecker heads has yielded some answers, among them a tightly fitted skull that keeps the brain from banging around and shock-absorbing muscles that encircle the skull.
The remarkable woodpecker finch is one of a group of fourteen finch species found only on the Galápagos Islands. Discovered by Charles Darwin in 1835, these birds, commonly called Darwin's finches, are very different from one another in feeding behavior and have beaks appropriately adapted to handle what they eat. Among them are species that feed on insects, seeds, leaves, nectar, or the pulp of cactus pads, according to David Lack. It is generally agreed that all of them evolved from a single colonizing flock of one species that somehow crossed 600 miles of the Pacific Ocean from the closest point on the South American mainland to the recently (geologically speaking) volcanically formed and at first lifeless islands. With few other birds to compete with them, they avoided competing with one another by evolving ways of exploiting unoccupied ecological niches.
An ornithologist working on the Galapágos in 1914 was the first to observe woodpecker finches using tools, Lack noted. Although they peck holes into trees to find wood-boring insects, they lack the long extensible barbed tongue with which true woodpeckers extract beetle grubs or other insects from their holes. Instead, as Sabine Tebbich and her colleagues reported, woodpecker finches “use twigs or cactus spines, which they hold in their beaks…to push, stab or lever [insects] out of tree holes and crevices…. Moreover, they modify these tools by shortening them when they are too long and breaking off twiglets that would prevent insertion.”
A few other birds, perhaps two or three dozen species, are known to use tools, but only a handful use them to capture insects. Jeffery Boswall noted three Australian birds—the shrike-tit, the grey shrike thrush, and the orange-winged sittella—that use twigs to probe for insects in crevices. In Tangipahoa Parish in Louisiana, Douglas Morse watched brown-headed nuthatches pry pieces of bark from longleaf pines with flakes of bark to get at hidden insects.
Nathan Emery and Nicola Clayton, in an article in a 2004 issue of Science, wrote that wild “New Caledonian crows…display extraordinary skills in making and using tools to acquire otherwise unobtainable foods.” Tools for extracting insect larvae from holes in trees “are crafted from twigs by trimming and sculpting until a functional hook has been fashioned.” Other tools, “consistently made to a standardized pattern” by cutting pieces from Pandanus leaves, are used “to probe for [insects] under leaf detritus [with] a series of rapid back-and-forth movements that spear the prey onto the sharpened end or the barbs of the leaf.” On foraging expeditions, the crows carry these tools from place to place. One caged New Caledonian crow, Emery and Clayton noted, appeared “to be capable of reasoning by analogy with her previous experience with hooks, by modifying nonfunctional novel material (metal wire) into hook-like shapes to retrieve food.”
In winter, cohesive flocks of black-capped chickadees, tufted titmice, nuthatches, brown creepers, golden-crowned kinglets, and downy woodpeckers wander through the woods foraging for insects. The birds, so to speak, gang up on the insects. Field studies summarized by Kimberly Sullivan “showed that individuals can benefit from membership in a flock by decreasing their risk of predation and increasing their foraging efficiency.” Flock members constantly sound contact, or social, calls—such as the chickadee's chick-a-dee-dee—that announce their presence and help to maintain flock cohesion. They also have calls, such as the chickadee's high-pitched zeee, that warn of an approaching hawk or other predator. Most small birds, according to Susan Smith, freeze or dive for cover in response to the warning calls of their own and other species. Sullivan, as we will see in chapter 9, found that downy woodpeckers spend much more time eating and much less time cocking their heads from side to side to watch for predators when they are with a flock than when they are alone, because the constant contact calls of their companions assure them that others are also keeping an eye out for predators.
Many of the 4,500 species of mammals—from tiny shrews, bats, and mice to huge bears—feed on insects to varying extents. Some, such as the African aardvark and the giant anteater of South America, eat nothing but ants and termites. Many omnivores, among them bears, raccoons, opossums, chipmunks, foxes, squirrels, mice, and skunks, include insects in their diets.
Primates such as lemurs, tarsiers, monkeys, baboons, chimpanzees, and humans are omnivores that, to varying degrees, feed on insects. In the early 1960s, Jane Goodall made the famous discovery that chimpanzees create tools from twigs and use them to “fish” for one of their favorite snacks, termites—the tropical species that build large cementlike mounds. Early in the rainy season, swarms of thousands of male and female termites of the reproductive caste leave the mounds through tunnels dug by workers, who keep the exit holes thinly sealed until conditions are favorable for the reproductives to fly off and found new colonies. When a hungry chimpanzee spots one of these lightly sealed holes, Goodall observed, it removes the seal with its index finger and pokes a tool into the hole. A moment later the chimpanzee withdraws the tool and then eats the termites clinging to it. Children in Africa use the same technique to get a few termites for a snack, but adults on the continent make ingenious traps to catch swarming termites—a much-favored food, delicious when roasted—by the thousands. As I explained in Fireflies, Honey, and Silk, people of almost all non-Western cultures eat insects, usually as a special treat.
Bats, the masters of the night sky and the only mammals capable of true flight, are not blind, but they find their way in the dark by means of echolocation (sonar). In flight they emit sounds too high-pitched for our hearing and sense obstacles and their prey, usually insects, by listening for the echoes that bounce back from them. As the Nobel laureate Niko Tinbergen observed, on what is to us a quiet summer evening, to the bats flying about and the moths that can hear them “the evening is anything but calm. It is a madhouse of constant shrieking. Each bat sends out a series of screams in short pulses, each lasting less than a hundredth of a second.” In chapter 9 we will consider the bat's echolocation in more detail and the question of how moths benefit from an ability to hear bats.
Shrews, which may weigh as little as a tenth of an ounce, are the smallest mammals on earth, and because of their tremendous metabolic rates—their hearts may beat 1,200 times a minute—they are the most voracious of the insectivorous mammals, and probably the most voracious of all mammals. Every twenty-four hours, a shrew eats the equivalent of its own body weight or more in insects, other arthropods, and occasionally a mouse or other small mammal. Shrews live and hunt in extensive runways at or just above ground level.
The mouse-size short-tailed shrew (Blarina brevicauda), common in the eastern half of southern Canada and the United States, is active both day and night throughout the year and is one of the world's few venomous mammals. Delivered in the saliva as the shrew bites, the venom is toxic to both small mammals, which this shrew seldom attacks, and insects, which are the most important part of its diet. The experiments of Irwin Martin showed that crickets and cockroaches are immobilized by the venom but do not die until three to five days after being bitten. “Venom,” Martin reasoned, “was therefore acting as a slow poison as well as an immobilizing agent. Immobilization for 3 to 5 days may extend the availability of fresh non-decomposing food, and thus enable Blarina to optimally exploit a sudden abundance of insects by caching some. If all hoarded insects were dead, many might [decay and] lose substantial nutritive value before the shrew could eat them.”
Insect eaters do, of course, help to prevent insect populations from soaring to ecologically disruptive levels—always a possibility because an insect, depending upon the species, will lay anywhere from a few to thousands of eggs. If, on average, two of a female's eggs survive to become reproducing adults, she will have replaced herself and her mate, and the population of her species will not increase. But if only an additional two survive, the population will increase by a factor of two in each generation and will soon become an ecologically disruptive force. Clearly, dozens or even thousands of a female's offspring must perish—and predators eat many of them.
The many insect-eating animals, from the little crab spiders to birds and even huge bears, consume enormous numbers of insects. In so doing, they exert the powerful selection pressure that results in the evolution of the many ways in which insects can survive by avoiding or defending themselves against predators. A few examples from agriculture show how great the selection pressure from predators can be.
In 1887, sap-sucking cottony cushion scales, insect invaders from Australia, infested California orange groves, threatening to destroy them all. Knowing that these scales were uncommon in Australia, where they were never destructive, Charles V. Riley, a great pioneering entomologist, reasoned that they were controlled in Australia by an enemy absent from California. He postulated that the scale population would crash if this enemy were introduced into California. Therefore a few hundred vedalias, ladybird beetles that eat these scales, were imported from Australia, and in less than two years only a small and inconsequential population of cottony cushion scales survived, coexisting with a few vedalias that kept them in check. In 1945, DDT, which kills vedalias but not the scales, was sprayed in the orchards to control another insect. As was to be expected, seriously destructive outbreaks of cottony cushion scales followed, but the benign balance of vedalias and scales was restored when the use of DDT was discontinued. Robert L. Metcalf and Robert A. Metcalf underscored the importance of predators in controlling pest insects with an example involving two native American insects. In 1899 in Maryland, in just a few days, sieves used in packaging fresh peas separated out twenty-five bushels of hoverfly larvae, which feed on aphids. “They were so abundant that they almost completely destroyed the pea aphids in the fields.”
In 1979, Richard Holmes and his coworkers showed that birds alone can significantly decrease populations of some plant-feeding insects. They covered plots of striped maple shrubs in a New Hampshire hardwood forest with nets that excluded birds but not insects. Nearby uncovered areas of similar size and with comparable growths of striped maple shrubs served as controls. The exclusion of birds, especially ovenbirds, black-throated blue warblers, veeries, and Swainson's thrushes, caused a significant increase in the numbers of leaf-eating caterpillars.
Similar experiments by Robert Marquis and Christopher Whelan in Missouri showed that insectivorous birds decreased the number of plant-feeding insects on white oak saplings by half, which in turn allowed the saplings to increase their aboveground growth by one-third. Like Holmes and his coworkers, they covered some saplings with nets that excluded birds and left other saplings uncovered.
Many of you have seen grasshoppers leap into the air and use their wings to make a speedy retreat when you come threateningly close to them. When I turn on the lights in my laboratory at night, panicked cockroaches swiftly run off to find a hiding place. (Entomologists can't use insecticides in their laboratories; insecticides kill not only cockroaches but also the insects that are the subjects of our experiments.) Many insects do not respond to most disturbances by fleeing, because they are camouflaged or hidden, perhaps on the underside of a leaf, under debris on the ground, or in some other nook. Some, however, will leave their hiding place to flee if an intruder comes too close—within a critical distance whose length will vary with the species of the prey insect. The next chapter considers running away and hiding as ways to escape from predators, to avoid becoming a meal for a bird, a mantis, a mouse, or some other insect eater.
