A Trickle-Down Forest Economy
by Edward S. Ross
A chattering and crashing of guenon monkeys in branches directly overhead—a sudden swish—a near miss! I was almost hit by a most unpleasant bomb—a monkey dropping. The fecal attack might have been deliberate—perhaps a normal defensive tactic in the world of primates. Adrian Forsyth, in Portraits of the Rainforest, amusingly noted that howler monkeys have a "bombs-away" attitude to this event, and they are not averse to anointing naturalists and other interlopers with their copious and pungent waste products. They are often quite good at targeting, and the combination of height and gravity gives their messages an impact that cannot be ignored.
The next morning in that Congo forest, I returned to the scene of the presumed bombing attack and much to my delight as an entomologist, I found the excrement crowded with colorful butterflies of at least 15 species, including those that normally fly high in the canopy. Joined by the other insects, they were bloating on fecal juices. Beneath the pile, scarab beetles were rapidly burying portions in the soil as provisions for their future larvae.
This activity reinforced my awareness of the nutritional importance to many insects of animal excreta and partially eaten fruit and prey that fall from a forest’s upper levels. In addition to such tidbits, all forests, both tropical and temporate, are primarily fed by another kind of "excrement"—a rain of soon-to-rot dead leaves, branches, and fruit. In deciduous, temperate forests, like those in the Washington metropolitan area, the drop is mostly seasonal, initiating a winter shutdown of the biotic factory. Because of winter’s cold and consequent long dormancy, there accumulates an ever-increasing amount of humus that ensures continued soil fertility long after an area is deforested.
In contrast, lowland, continuously wet tropical forests produce day and night, season after season, and many haven’t shut down for millennia. In portions of the Amazon Basin, for example, the production has been constant for perhaps 100 million years or more. Thus there has been time, warmth, moisture, and space for the evolution of a mind-boggling, seemingly impossible complex of species, especially of plants and insects. As the late Marston Bates so aptly stated, "almost anything can survive [in a tropical forest] and almost everything does."
Unlike in temperate forests, however, detritus in tropical forests is consumed by plants and animals shortly after it reaches the ground. Very little accumulates; it is truly a hand-to-mouth bioeconomy. Thus, most of the tropical forest’s life—its biomass—is above ground whereas that of a temperate forest is both above and below ground. This, of course, explains why rainforest soils, unless volcanic in origin, are too poor for sustained agricultural use and the forests are best left undisturbed.
As an entomologist, I especially appreciate tropical forests with a rich fauna of canopy vertebrates, particularly many birds. This is because of the large numbers and diversity of ground- and shrub-level insects that depend, for at least a part of their diet, on excreta falling from a forest’s upper levels. It follows, therefore, that the larger and more diverse the vertebrate fauna are, the richer and better fed many elements of the insect fauna will be.
Especially noticeable are insects, often in multi-species assemblages, feeding on juices of bird droppings. At least in the case of butterflies and day-flying moths, the attraction isn’t always food per se but, instead, dietary-enriching chemicals such as calcium and salt, which are in short supply in tropical forests due to leaching by heavy rainfall. Thus, in a sense, bird droppings function like the salt licks frequented by mammals in Africa. After a day of sweating in a humid forest, a visitor soon notes that he or she too has become a salt lick, with bolder insects imbibing salty perspiration on the skin and increasingly rancid clothing.
Skipper butterflies are especially attracted to bird droppings. These must primarily be visually detected, for swift, big-eyed skippers rapidly check anything white, even a fallen flower petal. When there is a scarcity of bird droppings, some skipper collectors bait leaf surfaces with guano-like pieces of tissue moistened with saliva. The saliva serves both as an adhesive and a dietary reward for the skipper, particularly if a collector has made it more attractive by sucking hard candy. Many other kinds of butterflies and insects are also attracted to such lures.
Most often, however, recognition of attractive detritus is by smell, not sight. I never cease to marvel at the sight of one or more insects feeding on a scarcely discernible caterpillar dropping, or the shriveled remains of a minute insect dropped by a bird. A faint column of odor rising from such bits appears to be detected by the many chemoreceptors, or sensillae, on antennae. The receptive insect then circles down and finally locates the morsel by sight. Very often other insects have already alighted on or near it, and their presence may lure even more insects.
Aside from these food sources, the most sought after and available nourishment for forest butterflies and other small creatures is not flower nectar, but fermenting fruit and sap oozing from stems and tree trunks. In the dark gloom at a rainforest’s ground level there are relatively few "insect flowers," that is, those colored to attract insects and shaped for their convenience, such as the daisy, which offers the insect a place to land. Most flowers within tropical forests are shades of red or orange that lure bird visitors, such as hummingbirds, during daylight hours. Many other flowers are white, often fragrant, and attract other pollinators, like long-tongued moths and bats, at night. Both types of flowers may secrete nectar in the depths of tubular corollas that can be secured only with a long tongue or proboscis during flight, or by "nectar thieves" that pierce corolla bases to steal nectar.
The adult activity of most butterflies is fueled by flower nectar. Egg production, however, is dependent on food reserves accumulated during the caterpillar stage. No eggs can be laid once those reserves are gone. Research by Thomas S. Ray and Catherine C. Andrews in Costa Rica, however, indicates that female ithomiine butterflies (a subfamily of Nymphalidae characteristic of New World tropics) can lengthen their reproductive life from a few weeks to at least four months by securing uric acid or partially digested proteins from the droppings. Frequent use of droppings as a dependable food supplement enables the butterflies to produce numerous egg clusters, perhaps throughout their lives. Because the droppings must be fresh, it is strategic for female ithomiines and other butterflies to frequent forest areas with an abundance of antbirds (family Formicariidae). Such birds fly above advancing hordes of army ants so as to feed on the insects the ants flush out of leaf litter and off low-growing plants. Researchers Ray and Andrews speculated that the butterflies locate bird concentrations by detecting the distinctive odor of masses of the ants.
Normally, birds are the primary predators of butterflies. Most ithomiines, however, have little to fear because the majority of adults, especially males, are likely to have ingested poisonous fluids (pyrrolizidine alkaloids) present in or on flowers and foliage surfaces of the very common plants of the tribe Eupatorieae of the daisy family. Thereby most have become distasteful, or even poisonous, to birds and other predators. This acquired repugnance is advertised by distinctive, interspecific warning colorations that are often mimicked by palatable, unrelated species. Adult ithomiines experimentally reared without access to poisonous plant secretions, including those of decomposing foliage of boraginaceous plants, are palatable. Most other unpalatable insects sequester protective toxins by ingesting during their larval stages foliage or sap of poisonous plants, such as Solanum (nightshade family, including tomatoes and potatoes), milkweeds, Aristolochia (Dutchman’s pipe), and Passiflora (passion vines).
Vertebrate predators don’t feed on excrement so a resemblance to such repugnant inedibles is a very common defense of many small creatures, such as some beetles, caterpillars, moths, spiders, and even frogs. Appropriately, as in so many other cases of object-resemblance, excreta-like creatures are adapted to remain immobile during the day with activity confined to the dark of night when most predators are inactive.
A curious twist occurs, however, when a bird-dropping resemblance not only serves as a defense but also as bait to attract prey. A remarkable crab spider in southeastern Asia not only appears to be a bird dropping, but also spins a white, flat web on a leaf surface that resembles splashed excrement. It then waits with trap-like fangs ready to snatch any salt-seeking insect that alights within reach. In this way, free-roaming white crab spiders may simply sit about fully exposed on leaves, luring insect prey without attracting the interest of vertebrate predators. Once I saw a fast-flying orchid bee (Euglossa), intent on getting nutrients from a real bird dropping, quickly caught and paralyzed as it alighted on such a spider. There also are pure white nymphs of assassin bugs (Reduviidae) that sit about for hours fully exposed with sticky forelegs widespread, ready to snatch fooled, nutrient-seeking insects.
Excrement is often mentioned as an important means of seed dispersal and this, too, can have interesting entomological aspects. True bugs (order Hemiptera), especially of the families Alydidae and Lygaeidae, regularly seek bird droppings containing seeds. Minutely barbed apices of their hair-like mandibles cut through seed shells and then macerate the contents while the bug injects salivary digestive enzymes that liquefy the solids so it can suck the predigested food. (Hemiptera subsist only on liquid food.) Because pre-oral digestion is a prolonged process that occurs while a bug is fully exposed to view on a leaf surface, the bugs reduce predation by mimicking ants, both in appearance and behavior—many predators avoid ants because they may sting, bite, or swarm their attackers.
Less subject to predation are tiny lygaeid bugs, Oligenes subcavicola, which form a great crawling mass, estimated at 400,000 bugs per square meter, on the floors of Neotropical caves. They subsist on billions of tiny seeds excreted by fruit-eating bats clinging to the ceilings of the caves.
At times attraction to a particular site isn’t due to animal excreta but instead to seepage of calcium and other useful chemicals inorganic in origin. A high clay river bank, a colpa, along Peru’s Rio Manu that attracts a multitude of parrots, including five species of macaws, is a famous example. It has been concluded that the birds obtain chemical antidotes to overcome toxins present in some of the fruits they eat. Dry season chemical concentrates on exposed bottoms and beaches of receding streams also can be very attractive to insect drinkers, especially if the stream has picked up salts while eroding upstream geological formations containing such chemicals. Primates, including humans, often chew such soil to obtain chemicals missing in their diets.
If a particular butterfly or moth drinking from such chemical-enriched soil is closely watched, one can often see sudden, regular ejections, even squirts, of fluid from the end of the abdomen. On impermeable surfaces, a small puddle may develop under the drinker. Obviously, fluid ejection results from a need to pass great quantities of soil moisture through the gut in order to extract a sufficiency of useful, but dilute, chemicals.
Sometimes a "puddle club," as they are called, can be quite amusing. In Brazil, I encountered a tandem line of three skippers on the ground, each rapidly squirting excess fluid from its anus. The second and third to the rear were in direct line to receive the full force of the squirts in their "faces," yet they didn’t move, even as liquid droplets piled up on their heads and bodies! Even better was a riodinid butterfly I observed sucking fluid from a bird dropping in an Amazonian forest. After a series of anal ejections it turned around and sucked up its own excrement!
Commercial butterfly collectors in Taiwan speed the accumulation of marketable specimens by pinning dead, damaged, or even paper butterflies, to urine-baited soil. Sometimes, near a tropical village, especially when a river bank is used as a latrine or a laundry, spectacular assemblages of butterflies may gather on the sand or mud, especially if the day is sunny. Curiously, butterflies often group within the multitude according to color and species. They fly up like confetti when disturbed and this might confuse a predator. Experienced entomologists hold their own urine for release where it will serve as bait on surfaces most convenient for collecting or photographing insects. Unless leached by rain, these sites will increasingly appeal to insects for several days as the urine ages.
Another trick is to concoct horrible, but effective, baits by mixing various ingredients such as stale beer, urine, fermenting fruit, and feces. After a period of "ripening," dabs of the disgusting gunk are placed here and there on various surfaces. Such bait would seem to be artificial, but most of its basic elements are highly nutritious. Most adult insects, in contrast to the specialized diet of their larvae, have rather broad tastes and are drawn to many strange foods, such as moist ashes, carrion, human saliva, eye secretions of turtles and mammals, aphid honeydew, sweet secretions of certain caterpillars, and fresh and putrefying fish. While I camped in Madagascar, great numbers of butterflies fed on our catsup. Interestingly, freshly emerged male butterflies are more attracted to such strange foods than are females.
Currently, most of my observations of insect behavior occur along trails in a large primeval forest reserve maintained by Butterfly Lodge (Cabanas Alinahui) on the upper Rio Napo of Amazonian Ecuador. Although more than 500 species of birds occur in the forest, their presence is more evident from their sounds and excreta than from actual sightings. Nevertheless, forest visitors are amply rewarded by first-time encounters with small creatures, especially beautiful butterflies, which so often concentrate on animal droppings and other detritus.
In spite of all this richness, I often think of how much more could be seen if the large mammal and bird fauna had not been shot out by local Indian and colonist hunters. The most significant loss has been monkeys, a favorite, easily hunted food—one almost a required entree on festive occasions such as weddings. Now, with monkeys so rare, I would willingly endure a "rain," or a deliberate bombing, of monkey feces, to be able to encounter an increase in excrement-dependent insects. What an experience it might have been to have seen tropical forests, or any other habitats for that matter, before that relatively recently evolved scourge—Homo sapiens—appeared on Earth’s scene.
Urgently, we must pay our debt to societies of plants and animals by supporting efforts to preserve and restore as many of Earth’s biomes as possible to serve as Louvres of Life, regulators of climates, watersheds, and sources of valuable products—some yet to be discovered. Not the least, such preservation will ensure that future generations of humans will be able to enjoy continued performances of ancient, life-enriching biodramas, each with its well-rehearsed cast of players, dramatically performed on Earth’s most lavishly decorated stage—the tropical rainforest.
Edward S. Ross is Curator Emeritus at the Department of Entomology at the California Academy of Sciences.
ZooGoer
27(5) 1999.
Copyright 1999 Friends of the National Zoo.
All rights reserved.
