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CALIFORNIA WILD

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Droppings From On High
In Tropical Forests Nothing Goes to Waste

A chattering and crashing of Guenon monkeys in branches directly overhead--a sudden swish--and a near-miss! I was almost hit by a most unpleasant "bomb." It was a monkey dropping. The fecal "attack" might well have been deliberate--perhaps a normal defensive tactic in the world of primates. Adrian Forsyth in his book, Portraits of the Rainforest, notes that howler monkeys have a "bombs-away" attitude toward intrusion, and are not averse to anointing naturalists and other interlopers. Primatologist Frank Carpenter saw the howlers' careful marksmanship as a sign of intelligence, remarking that "an individual would slowly approach to a place directly above me, or as nearly as possible, and then would release...."

Next morning in that Congo forest, I returned to the scene of the presumed attack and found the excrement crowded with colorful butterflies. There were many species jostling together including some that normally fly high in the canopy, well beyond the reach of a collector's net. They had been joined by flies and other insects, while, beneath the pile, scarab beetles were rapidly burying portions in the soil: provisions for their future larvae.

For many insects, the nutritional value of animal excretions, as well as partially eaten fruit and prey, falling from the upper levels of the tropical forest, is crucial to their survival.

Especially prevalent are insects, often in multi-species assemblages, feeding on fluids in bird droppings. For butterflies and day-flying moths the attraction isn't always calories. Sometimes it is chemicals, such as calcium, in short supply in tropical forests because of their dilution by heavy rainfall. In a sense, bird droppings and other excreta create licks comparable to salt licks in Africa's grasslands. After a day of sweating in a humid forest, an observer soon discovers that he or she too has become a salt lick with bolder insects imbibing perspiration on the skin and increasingly rancid clothing.

For many forest butterflies and other small creatures, the most available food is not flower nectar but fermenting, fallen fruit and sap oozing from stems and tree trunks. In the dark gloom beneath the rainforest's canopy, there are relatively few "insect flowers,"--those that are colored to attract insects and shaped for their convenience. For instance, in open habitats, some flowers, such as daisies, offer a place to land. Most low-level flowers are colored red or orange to lure birds, such as hummingbirds, during daylight. Many other flowers are white, often fragrant, and attract long-tongued moths and bats at night. Both types of flowers generally secrete nectar in the depths of tubular corollas which can be reached only with a long tongue or proboscis during flight; or by "nectar thieves" that pierce corolla bases to steal it.

Skipper butterflies are especially attracted to bird droppings. Swift, big-eyed skippers check anything white--even a fallen flower petal. When there is a scarcity of bird droppings, some collectors of skippers bait leaf surfaces with guano-like pieces of white tissue paper moistened with saliva. The saliva serves both as an adhesive and a dietary reward for the skipper--particularly if the collector has been sucking hard candy.

Research by Thomas S. Ray and Catherine C. Andrews in Costa Rica indicates that female ithomiine butterflies can lengthen their reproductive life to at least four months by securing uric acid or partially digested proteins from bird droppings. Most other butterflies are restricted to food reserves accumulated during their caterpillar stage, and their egg production is limited. Flower nectar fuels only their adult activity. Ithomiines, however, thanks to the use of bird droppings as a food supplement, can produce numerous egg clusters perhaps as long as they live.

Because the droppings must be fresh, ithomiines and other butterflies tend to frequent forest areas with an abundance of antbirds (family Formicariidae). These birds fly above advancing hordes of army ants and feed on 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 ant masses.

Birds are the primary predators of most butterflies. Ithomiines, however, have little to "fear" because the majority of adults, especially males, are likely to have ingested poisonous fluids (pyrrolizidine alkaloids) present in flowers and on the surfaces of species of Eupatorieae--common members of the daisy family. In the process the butterflies become distasteful, even poisonous, to predators. They then advertise this repugnance by distinctive warning colorations which, in turn, are often mimicked by edible, unrelated butterflies and moths. (Adult ithomiines experimentally reared without access to poisonous Eupatorieae secretions, including those of decomposing foliage of boraginaceous plants, are palatable.)

As you might suspect, most insects recognize dietary detritus by smell, not vision. 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 rising odor appears to be detected by the many chemoreceptors, or sensillae, on antennae. The receptive insect circles down until it finally sees the morsel. Very often other insects have already alighted on or near it and their presence lures yet more insects.

Obviously, vertebrate predators don't regard excrement as food, so 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 imitators are adapted to remain immobile during the day, their activity confined to the hours of darkness when most predators are inactive.

But some predators play that game, too. They attract prey active during the day by mimicking bird droppings. A remarkable crab spider in southeastern Asia not only looks like a bird dropping, but the spider also spins a white, flat web which resembles a dropping splashed on the leaf. The spider waits, without fear of predation, its trap-like fangs ready to snatch any salt-seeking insect that alights within reach. Once I watched as a fast-flying orchid bee (Euglossa), intent on getting nutrients from what it took to be a bird dropping, alighted on such a spider and was quickly caught and paralyzed. Pure-white nymphs of assassin bugs (Reduviidae) sit about for hours fully exposed, their sticky forelegs widespread ready to snatch fooled, nutrient-seeking insects.

There are also significant entomological aspects to the importance of excrement in seed dispersal. True bugs (order Hemiptera), especially of the families Alydidae and Lygaeidae, regularly seek bird droppings containing seeds. Minutely barbed tips of their hair-like mandibles cut through seed shells. Into the shells they inject salivary digestive enzymes that liquify the solids so that they can be sucked up. (Hemiptera subsist only on liquid food.) Because this prolonged process is fully visible on a leaf surface, the bugs reduce their vulnerability by mimicking ants, both in appearance and behavior.

Less subject to predation are tiny lygaeid bugs, Oligenes subcavicola, which can compose great crawling masses on the floors of neotropical caves, estimated at 400,000 individuals per square meter. They subsist on billions of tiny seeds excreted by fruit-eating bats clinging to the ceilings of the caves.

Soils containing liquid excreta, notably urine, are also popular, for they are often sites of concentrated chemicals. If a particular butterfly or moth drinking on these soils 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 sufficient useful, but dilute, chemicals. This has its parallel in a beer drinker's need to frequently visit the restroom.

Sometimes a "puddle club" can be quite entertaining. Recently 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 full force of squirts in their "faces," yet they didn't move, even as droplets piled up on the head and body. Even more surprising 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 excretion.

I have seen commercial butterfly collectors in Taiwan speed the accumulation of marketable specimens by pinning dead, damaged, decoy butterflies, or even paper butterflies, to urine-baited soil. Sometimes, near a tropical village, especially when a river beach is used as a latrine, or a laundry, spectacular assemblages of butterflies may gather on the sand or mud, especially on sunny days. Curiously, butterflies often group according to color and species. They fly up like confetti when disturbed, perhaps to confuse a predator. Experienced entomologists hold their own urine for times when it will serve as bait in places most convenient for collecting or photographing. 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 splattered on suitable spots. 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 catholic tastes and are drawn to many strange "foods," such as moist ashes, carrion, saliva, eye secretions of turtles and mammals, aphid honeydew, sweet secretions of certain caterpillars, and fresh and putrefying fish. While we were camping in Madagascar great numbers of butterflies fed on our catsup. Freshly emerged male butterflies are especially attracted to such strange foods.

Currently, most of my observations of insect behavior occur along trails in a large virgin rainforest reserve maintained by Butterfly Lodge (Cabanas Alinahui) on the upper Rio Napo of Amazonian Ecuador. Although more than five hundred species of birds occur in the forest, their presence is more evident from their sounds and excreta than from actual sightings (see Pacific Discovery, Spring 1993). Nevertheless, a forest visitor is amply rewarded by first-time encounters with small creatures, especially beautiful butterflies, often concentrated on animal excreta and other detritus.

In spite of all this richness, it would be much richer if many of the large mammals and birds had not been shot out during the last few decades by local Indian and colonist hunters. The most significant loss has been the monkeys, a favorite, easily hunted food--almost a required entree on festive occasions such as weddings. However, howler monkeys can be heard in the distance, and guests at Butterfly Lodge can have the satisfaction that a portion of the cost of their stay contributes to a fund, maintained by Health and Habitat of Mill Valley, California, to purchase thousands of additional acres of forest which will encourage and safeguard a primate fauna. Personally, I would willingly endure a "rain," or a deliberate bombing, of monkey feces, to gain the ensuing increase in excrement-dependent insects.

Edward S. Ross is Curator Emeritus of entomology at the California Academy of Sciences.

Summer 1996

Vol. 49:3