Singing Caterpillars

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Several issues ago we took a look at the remarkable transformation of caterpillar to butterfly (“The Butterfly: Master of Metamorphosis,” January-February 2018). But this humble creature has far more surprises in store for those willing to look more closely.

In a number of tropical areas, most notably South America and Australia, one may have the privilege of encountering a midsize butterfly of the Lycaenidae or Riodinidae species. These beautiful creatures can range in colour from copper to shades of blue. But while their entrancing colors and peaceful demeanor may be delightful to behold, the story of how these two specific species survive to grow into such graceful butterflies is perhaps more amazing still.

A butterfly spends a large part of its early life in a larval stage, a form we know as a caterpillar. In that phase it is slow-moving, vulnerable to attack and becoming the dinner of other species. Butterfly larvae are especially vulnerable to wasps, whose own larvae seem to relish a diet of caterpillar. Wasps will hunt and capture these caterpillars, and lay eggs inside their bodies. Then, when the eggs hatch, the wasps’ young will consume the caterpillars for their own development.

The Lycaenids and Riodinids, however, do not easily become a feast for wasps, due to a remarkable “partnership” with various species of ants, which end up serving as aggressive bodyguards for our lumbering larvae.

A Remarkable Partnership

Biologists have done much research over the past 40 years on this special interspecies relationship and how it came about. Such a partnership between creatures is called a symbiotic relationship (from a Greek word for “living together”), and the equipment and processes involved in this particular arrangement are truly stunning. Phil DeVries, writing for Scientific American in October 1992, described some of the fascinating ways these caterpillars attract and retain ants to serve as their guardians.

DeVries explains how a caterpillar of these species produces sound by scraping a ribbed vibratory papilla (protrusion) against the rough surface of its head. The resulting vibrations carry among the tree branches so any ants in the vicinity may hear them—hence the nickname “singing caterpillars.” These vibrations just happen to have a similar frequency to the vibrations that the ants themselves make when they wish to communicate the location of a newly discovered food source—so, naturally, the other ants come running.

Because ants have been known to prey upon caterpillars, it would appear as though our friend is playing a dangerous game. However, the caterpillar is not unprepared. Toward its rear end, it has a nectary organ that secretes a sugary, protein-rich nectar which happens to be an ideal food source for ants. Seemingly aware that they have come upon a culinary motherlode, the ants guard the caterpillar from other predators, “milking” it by tickling or drumming on the secretion glands with their antennae. Sue Ann Zollinger writes, “In some Australian species, the attending ants even build thatched or earthen corrals to contain the caterpillars. By day the caterpillars are protected from predators by the corral and the ants. At night the ants herd the caterpillars up a nearby tree to feed on leaves” (“The Special Relationship Between Ants and Lycaenid Butterflies,” A Moment in Science, September 15, 2008).

The ants are even able, in many cases, to defend against birds! If a bird or larger predator approaches, the ants swarm over the caterpillar. Most birds consider ants to be foul-tasting, so the sight of ants on the potential meal repels them—and, thus, the caterpillar is spared.

Some of the ants’ behaviors, however, have puzzled researchers. For instance, a University of Arizona publication reported that ants will often defend certain nectar-secreting plants by attacking—and sometimes eating—other insects, thereby keeping the food source just for themselves. However, the ants give a pass to nectar-producing caterpillars, allowing them to eat the plant. Meanwhile, the ants milk the caterpillars’ nectar and fight off potential threats (Stiles, Lori, “To Tend or Not to Tend: The Choice Varies in an Ant-Butterfly Mutualism,” August 7, 2000. Arizona.edu). Other research indicates that the caterpillar’s nectar is more nutritious than that of the plants (DeVries and Baker, 1989, Journal of the New York Entomological Society 97: pp. 332–340). Interestingly, as Stiles reports, “The caterpillars will only secrete the substance [nectar] when ants are there.”

Commanding a Private Army

Ms. Stiles further observes that at different times, the caterpillars’ pores secrete substances that appease or excite the ants. In addition, on its eighth abdominal segment, the caterpillar has a pair of tentacle-like organs which are somewhat balloon-like and covered with fine hairs, and it uses them in a remarkable way. Ants get very agitated when they touch these organs, and it seems that the caterpillar uses them to manipulate the ants, making them defend it when needed and sending them away when they are not.

So, on the surface, the caterpillar seems to receive protection from the private army of ants it has attracted, while simply providing delicious nectar in return. This is impressive in itself. However, biologists have discovered this relationship to be more complex, and that the caterpillar is designed with the ability to control the ants!

In 2015, Sandhya Sekar reported for New Scientist magazine on the work of Japanese scientist Masaru Hojo. The biologist noted early in his work that the ants defending the caterpillar did not leave it, even to take food back to the colony. Instead, they remained on guard duty and drank nectar. He noted that, “whenever the caterpillar everted its tentacles—flipped them so they turned inside out—the ants moved around more rapidly, acting aggressively” (“Caterpillar drugs ants to turn them into zombie bodyguards,” July 2015. NewScientist.com). In this mode, the ants attacked wasps, spiders, and any other threat. Hojo speculated that the caterpillar, when approached by a possible predator, gave a chemical signal ordering the ants to attack, thus dictating their behavior through both chemical control and powerful nectar. Experimentation showed that the caterpillar can “spike” its nectar with drugs to control the dopamine levels in the ants’ brains, making its bodyguards more or less aggressive as it wills.

What Professor Hojo discovered is truly amazing. He demonstrated that Lycaenidae or Riodinidae, relying on ants for their security, use chemical controls to cause the ants to do their bidding. Their nectar can calm the ants, entice them to stay around, and make them aggressive enough to fight off dangers (Hojo, Pierce, Tsuji, “Lycaenid Caterpillar Secretions Manipulate Attendant Ant Behavior,” Current Biology, 2015).

In order for this relationship to have ever begun functioning in the first place, these caterpillars would have had to be able to attract ants, produce desirable nectar (which they use only to feed defender ants), control the ants they attracted, and avoid being eaten by the rest of the colony. This would have required advanced knowledge of sound frequencies (especially those the ants use to communicate) and enough expertise in biochemistry to create tasty nectar and drugs capable of calming or exciting attendant ants at will. To suggest that such a complex arrangement could have been accidentally developed by random, minute evolutionary steps defies both reason and probability. What we see in these “singing caterpillars” is clear evidence of deliberate design and the production of fully functional creatures, made with an intricacy that is nearly impossible for mankind to comprehend.

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