The Blues - Summer World: A Season of Bounty - Bernd Heinrich

Summer World: A Season of Bounty - Bernd Heinrich (2009)

Chapter 7. The Blues

IT’S 12 MAY AND I’M AT CAMP IN MAINE. MR. WITHAM, who lives alone in a shack at the bottom of the hill, tells me that the ice was still on nearby Hills Pond last Friday. But today I heard the loons from that direction, so there is probably finally some open water. There is still snow along the roadsides, although the recent warm days have greened the aspens on some of the hillsides. Leaf-eating caterpillars are already on the trees, because swarms of warblers, vireos, and red-breasted grosbeaks arrived, almost to the day, as soon as the trees unfurled their leaves. It is warm and sunny enough today for the red Formicidae ants that live in and around my cabin to be active as well. They were running in a column up and down the trunk of the birch tree next to the cabin. A couple of the ants in the column were dragging a small caterpillar. I took it from them, and identified it as a species of “prominent” (notodontid) larva that I had in previous years found feeding on birch leaves. I then returned it to the base of the tree, and within seconds four or five ants almost pounced on it. But my most memorable sighting today was a tiny butterfly, Lycaenopsis argiolus, the spring azure. This butterfly is not uncommon when the poplars leaf out, and I may see more than one on any walk along the path up to my camp. The spring azure’s common name is apt, because this is the first butterfly to emerge from pupae that hibernated all winter (some, like the mourning cloak butterfly, overwinter as adults). It is hard not to be entranced by this butterfly. The surfaces of its sky blue upper wing glint like mirrors of the sky as it flutters over last year’s pastel-colored dead vegetation seeking the first spring flowers, often while there are still patches of snow on the ground. When the azure flies, there has been warm weather before it, and summer is not far behind.


Fig. 17. The spring azure and one of its pupae. The caterpillar is sluglike in form and is tended by ants.

The spring azures’ green sluglike caterpillars feed on buds and flowers of violets, and they are usually “tended” by ants. Ants kill most other caterpillars with little hesitation, yet they do not eat these caterpillars. Instead, they associate with them and repel predators as well as insect parasitoids, effectively acting as the caterpillars’ bodyguards. The secret of the caterpillars’ allure to the ants is that the caterpillars exude droplets of a sweet, protein-rich nutrient broth from glands on their backs when palpated by the ants’ antennae, and the ants lap this broth up.

MOST MEMBERS OF THE AZURES’ LARGE AND VERY INTERESTING family of butterflies, loosely called “blues” (although not all of them are blue), have small sluglike caterpillars. Few people except experts and aficionados (most famously including the novelist Vladimir Nabokov), who have studied them sufficiently to be able to distinguish them and name new species, know where to find them. But ants and these caterpillars find each other.

Many blues caterpillars are renowned for their close association with ants, and unlike the vast majority of caterpillars, some of these feed ants as the azure does, others move into the ant nests and are there fed by ants, and still others move in with the sheltering ants and are carnivores of their young. One thing has led to another in a likely evolutionary progression.

Once an organism has “found” or invented a successful strategy, the stage is set for replication, amplification, and modification. The great species diversity of the blues probably arose because an ancient ancestor had hit on the ant guard, thereby creating a new, safer niche for itself—one less exposed to birds and other predators as well as parasitoids. It is not likely that thousands of species of blues each independently discovered ants, but they have done different things with ants, and vice versa. Some of the most intricate and interesting associations are found in the nearly perpetual summer of the tropics.

One of the species most highly differentiated from its ancestral condition (evolved) is the moth butterfly, Liphyra brassolis, a huge Asian and Australian “blue” with a wingspread of nearly three inches. It is a relative of all other blues, but it is colored brown and black. In this butterfly the larvae make the ultimate use of ants: they are protected by living inside the nests of a very aggressive tree ant, Oecophylla smaragdina, and then they eat the ants.

These ants’ nests are made by cooperation between the young and the adults. The larvae produce silk thread from their salivary glands, and an adult holds a larva in its mandibles and waves it back and forth between two leaf edges. As the larva exudes its sticky silk, it attaches to the leaves, which become glued together to produce the shelter that is the nest—the shelter that the butterfly larvae then use as well. But how do the butterfly larvae gain entrance to the ants’ citadel? What we see now is a result of a long evolutionary arms race, a contest that these caterpillars have apparently won, because they get all the benefits whereas the ants gain nothing. Presumably, as with the spring azure in Maine, the caterpillars were originally symbiotically or at least benignly associated with ants.

The exact steps from there to here are obscure, but details of life histories suggest the problems faced and the possible solutions. At present the moth butterflies lay their eggs on the underside of branches, where they are less likely to be detected, and then the young caterpillars crawl into the leaf nest on the twig high in the tree. Undoubtedly they suffered casualties for millions of years, but over that time they evolved a thick leathery skin that ultimately became a nearly impenetrable armor and transformed the originally sluglike form of the blue’s caterpillars into a little tank. The armored caterpillars are equipped with “treads” that allow them to attach themselves to the ant’s nest substrate, primarily the leaf surfaces, so that the ants can’t turn them over and bite into their soft underbellies, and can’t detach them to throw them out.

The problem comes when the caterpillar must molt to the pupal stage, since the fresh pupal skin is necessarily soft, thin, and easily penetrable. However, these caterpillars have solved that problem, too. When they molt to the pupa they remain inside the caterpillar-tank skin, rather than discarding the skin as all other caterpillars do. But staying encased in the armor could be a problem later on, when the adult needs to emerge. To solve the problem of getting the tough armor off, the caterpillar shell has built into it predetermined lines of weakness that allow the soft, emerging butterfly to more easily crack out of the tank. However, the adult butterfly emerging within the ant nest is still necessarily soft; otherwise, it could not expand or inflate its wings, and it could then potentially be dispatched by the ants. Again, the butterfly has a special solution—unlike other butterflies, this species is covered with a dense layer of white, mothlike, powdery scales (hence the name “moth butterfly”) that gum up the mouthparts of any ants trying to bite it. The loose scales stay on long enough for the soft, still vulnerable butterfly to escape the ant nest and then inflate its wings and harden its cuticle outside the nest. The rest of the protective powdery scales are eventually sloughed off on their own.

The Oecophylla ants that host these caterpillars are very aggressive, and so they are all the more useful to any caterpillars that can breach the ants’ defenses. These day-active ants are also aggressive toward other ant species and try to evict them from their trees (kill them) whenever possible. Yet another ant species, Polyrhachis queenslandica, may live on the same tree with the Oecophylla. It avoids overlapping by being strictly nocturnal. In the daytime, when the Oecophylla are active, the Polyrhachis avoid being killed by staying in their nests—a couple of superimposed leaves glued together and sealed along the sides, with only two narrow tubelike entrances built into opposite ends of the nest. During the daytime, guard ants position themselves at these entrances and neatly plug them with their flat heads. No Oecophylla can get past these head plugs to enter, nor can any caterpillars. Nevertheless, these ants also host a blue caterpillar—one that has evolved a strategy exactly opposite that of the moth butterfly.

This blue, Arhopala wildei, lays its eggs directly on the Polyrhachis queenslandica ant nests or on twigs near one of the two nest entrances. To these ants, the caterpillars are not enemies; but their Oecophylla enemies on the same tree would eat them. To avoid that fate, these blues’ eggs hatch at night when the Oecophylla sleep, and the nocturnal Polyrhachis ants then safely carry the young caterpillars into their nest before dawn. Once inside they treat these blues’ caterpillars as their own larvae, and when the caterpillars molt the ants even assist them by pulling apart the cuticle to help them emerge, in the same way that they help their own larvae to molt. And if the nest is disturbed the ants carry the caterpillars to safety along with their own brood. The bribe? The A. wildei caterpillars have a gland on their posterior end that produces an ambrosial (to the ants) exudate. The caterpillars offer this tasty treat by raising their rear end to allow direct access to it whenever an ant approaches them. Apparently they have a scent that mimics that of the ant larvae so that the caterpillar is confused with one of them. Meanwhile, the treat ultimately comes from the ants themselves, because the caterpillars gorge themselves on the ants’ eggs, larvae, and pupae.

There is so far no explanation why these blues’ life cycles are so much more complex than that of the familiar azure that ushers in the short summer in Maine. But perhaps in a perpetual summer, such as a tropical one, there is more time and opportunity to evolve complex social relationships.

By far the majority of the larvae of the world’s butterflies and moths feed on leaves, often the plentifully available leaves of trees, and one might not expect that much sophistication and intrigue might be involved in the behavior of harvesting them. But, as the blues indicate, one should never underestimate even a caterpillar!