In defense of caterpillars: underappreciated and under attack, caterpillars also have to contend with freeloaders

Natural History, Dec, 2001 by Lee Dyer

The protagonist of Eric Carle's illustrated children's book The Very Hungry Caterpillar is what we all expect a caterpillar to be: a green, wormy eating machine that someday will be transformed into something better, such as a butterfly. Most people's attitudes toward caterpillars are based on this sort of lowly image and range from distaste (for, say, large hornworms munching on tomatoes in the garden) to indifference (toward, say, buckeye larvae chomping on weeds). The truth is that most leaf-eating caterpillars are not little green slugs. The amazing array of caterpillar colors, shapes, appendages, and behavior rivals that of their adult counterparts, and in many cases the immature organisms are far more pleasing to the eye.

Caterpillars evolved in response to a wide variety of selective pressures, but perhaps their most interesting features are adaptations against natural enemies. The value of defenses such as spines or sticky hairs, the regurgitation of plant toxins on an enemy, and the ability to mimic a snake is easy to imagine. But investigations into just how effective these defenses are--and against which enemies--reveal complex, unexpected patterns.

The vast and varied cast of characters that make their living by eating insect larval tissue includes a wide range of organisms, from microbes to primates. Two well-studied groups of caterpillar enemies are predators (many birds, wasps, ants, and true bugs) and, more obscure but no less abundant or important, parasitoids--certain wasps, flies, and nematodes whose immature stages live inside the caterpillar host, where they feed on nonessential tissues until they are ready to burst out of the devastated body and complete their life cycle as free-living organisms. Their gruesome predilection makes parasitoids great fodder for science fiction movies, but they benefit some plants by controlling populations of caterpillars.

Given the damage this sort of parasitism can cause, I expected that many defenses in the caterpillars' repertoire would have evolved in response to it. Surprisingly, however, my research, done at Tulane University with my former postdoctoral collaborator Grant Gentry, suggests this is not the case. While sticky hairs that glue an ant's mandibles together and toxic chemicals that make birds vomit can effectively deter predators, it turns out that parasitoids are actually attracted to caterpillar hosts with these attributes.

At first this finding confused us, because some of these larval defenses are formidable and have been demonstrated to affect parasitoids. Closely spaced spines, for instance, can make it harder for a parasitic wasp to lay its eggs on the caterpillar's body. And the toxins with which some caterpillars defend themselves against predators can also slow the development of, or even kill, parasitic larvae.

But we soon realized that the parasitoids' attraction to well-armed hosts makes good sense. Any parasitoid inhabiting a defenseless caterpillar becomes just as vulnerable to predators as its host is: if the larva is eaten, the parasite will be consumed right along with it. Far better, then, to parasitize a well-defended host, despite the cost. Thus, it appears that as long as caterpillars are challenged by both attackers from without and freeloaders from within, the perfect defense may elude them.

A giant tropical ant (Paraponera clavata) can inflict a vidous sting, strong enough to immobilize prey. But the sticky hairs on a Tarchon moth larva prevent the ant from properly grasping its prey and delivering its stinging message.

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Heliconius hecale zuleika, a caterpillar in the long-winged butterfly family, stores toxins from the plants that it eats; it also advertises its toxicity to experienced predators in black and white. An enemy that ignores the conspicuous warning is liable to be met with a nasty blast of regurgitated plant compounds.

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The mandibles of P. clavata are rendered temporarily useless by a mouthful of sticky hairs, courtesy of the intended prey. Sticky hairs don't work as well against most parasitoids, whose larvae grow inside and ultimately kill their caterpillar hosts.

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Agaraea larvae feed en masse: Group feeding can reduce an individual caterpillar's exposure to predators and enhance defenses such as thrashing and biting. One downside of group dining is that chemical signals from the larvae and their frass (excreta) can attract parasitoids. Some species of larvae eject their frass great distances to avoid discovery.

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Many caterpillars are cryptically colored to match their host plants, making it difficult for birds and reptiles to spot them. But those predatory insects that locate prey through chemical sensing are not deterred. Using caterpillars such as this well-camouflaged Adelpha, the author and his collaborators have reared a plethora of fly, wasp, and nematode parasitoids.

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Acharia ophelians, a saddleback caterpillar, has stinging spines and perhaps other chemical defenses that are advertised by its bright coloration. Brush up against a group of these, and you could have a painful rash for more than a week.