Chapter I. The Terebinth Aphids.

Jean-Henri Fabre Mason-bees

Winged female aphid (alate)

Assisted by luck, the animalcule attains its winter refuge, attaches itself by means of its stylets, imbibes and in turn founds a colony itself, but with less zeal apparently than its predecessors, who were blessed by the heat of the summer. By the same method of rapid procreation employed by its predecessors, that is, live birth without sexual intercourse, it surrounds itself with a modest tribe of offspring that ultimately take the form of black, alate aphids, like the ones that we saw previously, emigrating from the galls.

Adept at flight, these too are travelers, but they take the reverse route of their predecessors. The former went from the terebinth to the fields, whereas the latter abandon the fields for the terebinth. They depart from their overwintering sites at the base of grasses to populate the bush where they will form galls, their summer residence. Being present to observe their arrival entails no difficulty whatsoever.

Daily, during the first half of May, I visit the terebinth in the hedge. The leaves of the bush are already unfurling, not yet having attained the green color of maturity. The majority of the leaflets are swelling at their tips, forming the shape of a little crimson pocket; this is the initial handiwork of the spring population. Around 10 o'clock in the morning, if the air is still and the sunshine is bright, the alate aphids arrive, coming individually from every direction. They alight on the foliage of the upper twigs and immediately start wandering around, searching. The crowd soon becomes quite large.

They march busily in broken columns along the branches and the trunk. The majority of the caravan heads from the top towards the bottom, evidence that the object of their search lies towards the ground. This general descent is quite noticeable, and it attracts one's attention right away. However, there are some individuals that are bucking against the current, or simply wandering aimlessly about. These are readily distinguished from the others by their truncated bodies, one would say that a surgery performed behind the third pair of legs has resulted in the loss of their abdomens. Extraordinary creatures, for sure! They are walking thoraxes. The descending individuals; however, have well-formed, almost pot-bellied, abdomens that are pale green ventrally. We will soon unlock the secret of the ones with the sawed-off look.

For now, let us continue to observe the plump individuals. They move about the smooth, bare bark, indiscriminately and without stopping. If they come across a rosette of a lichen, they stop there for a few moments. Since lichens are found in greatest abundance at the base of the bush, on the trunk, this is likewise where the descending column tends to orient itself. The yellow rosettes of the lichen are soon covered by these visitors, who, pausing briefly, then proceed to insert the tip of their abdomens between the scales. The events unfolding under the cover of the lichen remain hidden from my eyes. As soon as their business is finished, which requires but a brief time, the aphids resume their march, but now they are shy an abdomen; they climb back upwards, they fly away. By one o'clock in the afternoon, all that remains on the bush are a few loiterers with truncated abdomens. For two weeks, as long as the weather remains pleasant, the same scenario recurs again and again.

What happened inside the mysterious innards of the lichens? Observations in cages will teach us. With the tip of a brush, I randomly brush some aphids from the downwards-marching group into a glass tube. I submit them to the violent obstetrics that I employed previously to examine the wombs of the autumn migrants.

With the back of a needle, I press the abdomen against a piece of paper. Without a single exception, they all yield a group of fetuses with black eye spots. Once again we have before us viviparous asexual procreators. All of them give birth indiscriminately, undeserving of the title mother or father.

They are mere birth sacs whose role is to airlift a new generation to the terebinth bush, one that so frail as to be incapable of getting there by its own means. Two alate forms, vehicles for the generation yet to come, shuttle from the grasses to the bush when the beautiful days and the season of mountain chalets arrive, and then from the bush back to the grasses and underground shelters, when the cooler days arrive. Garbed in like manner, nearly identical in shape and size, the two alate forms are moderately fecund. The autumn migrants carry a half dozen immatures; the reproductive capacity of the spring migrants is likewise in this range.

Now that we have witnessed abdomens emptied under the pressure of a needle, let us now let matters run their normal course. I brush some winged aphids, downward-bound from the apical regions of the terebinth, into a glass tube. I give them a dry twig from the bush as a field for exploration. Almost before you know it, things start happening. In less than a quarter of an hour, the captives give birth. It is here, in front of my window panes, that the autumn migrants have shown us their haste. Once their time has come, birth takes place on the first surface that they encounter, suitable or otherwise. Thus the arrivals at the terebinth make haste to descend to the base of the trunk, carpeted with lichens, a refuge par excellence. If they are delayed in getting there, they empty their sacs on the way, with great danger to the young who are then left without shelter.

For now, the twig with which I furnished the tube represents the bush. With alacrity the winged aphids move all over it, populating it with their young. They stop only long enough to deposit them, one by one, here and there, at random. They are machines that expel their products with the consummate indifference of insentience.

Like those of the fall generations, the young are born on end, glued by their backs to the substrate, and wrapped in a diaper so fine that it is barely visible under a magnifying glass. For a few minutes the infant remains immobile, and then the wrapping tears, and the legs free themselves. The little beast sheds its wrapping, tumbles right side up and goes on its way. The world is now richer by one more aphid.

After a few minutes, the flanks of the parent dry up, and all of a sudden the sower of infants is hardly recognizable. The bag of fetuses, formerly replete, shrinks so much that it ejaculates its remaining contents and ends up as an insignificant granule. The animal is now nothing more than a winged thorax. Now we have the solution to the enigma posed to us by the double procession of aphids on the terebinth. The descending caravan, with distended bellies, went to the lichens to deposit their loads of young; the ascending caravan returns, deprived of their abdomens after having given birth. The ultimate goal of the sojourns on the scaly rosettes of the lichens was thus the deposition of offspring.

For proof, I collected some pieces of lichen. There, crouching in great numbers under the cover of the scales, I found the same minute creatures that I obtained in my tubes in as great quantities as I could wish for. Let us add that, now that the act of birth is completed and the abdomen vanished, the alates perish in a day or two. Their role is finished.

Whether born in my tubes or extracted from their natural shelters, the little lice fall into four categories, each morph readily distinguished by its coloration. The most numerous are grassy green, with pale, colorless heads and legs. Their shape is somewhat lanky, slender. The others, two to three times larger than the former, are pot-bellied. Among the latter, there are some that are pale with a faint yellowish tinge; others of a pronounced amber color, and finally, some that are bright green.

An individual alate aphid will give birth in its litter of six to eight to both the slender morphs, always green, and the pot-bellied morphs, all of which may be amber colored, pale, or also green. It is very probable that these three colors are representative of different species. Nevertheless, I can observe no differences in the general characteristics among the alate aphids that birthed them. I would no doubt find them; however, if I did not balk at the idea of the tedious details of a microscopic examination.

Let us now get to the most interesting facts. No matter what their color, all of the young aphids are lacking stylets and endowed with two very distinct black eye spots. Thus, they can see, they can navigate, search, and congregate; but they take no nourishment, as attested to by the complete absence of a proboscis.

They actively wander around the terebinth twig with which I have furnished the tube in which they were born; they stop at the fissures in the bark, enter them, and explore them, and then resume their busy wandering. Finally they take refuge at the two ends of the broken twig. There, among the interstices between the separated wood fibres, they crouch down, the rump end sticking out, and their heads buried in the fissures.

The next day I find the majority of them assembled on the wadding that stops up the tube, which more or less approximates the hiding places in the lichens. There they remain motionless. Between long intervals; however, I perceive some that gently wave a leg, I see them pairing up, the slender morph on top, the pot-bellied morph on the bottom. It's now obvious what is happening: this time, I finally have the two sexes under my scrutiny, the two true sexes, and I am observing mating. The male is the smallest, always green colored, the female is the larger, each species a different color. What cold lovers! What marriages! At the most, now and then, the antennae tremble and the feet stir. For about an hour the two paired atoms remain entwined, then they take their leave of one another. It's finished.

At first I don't dare believe what my own eyes are witnessing, confronted with miserable nuptials such as these. As a rule the nubile age is a flowering. To celebrate their weddings, insects transfigure themselves, they acquire more robust, elegant forms, they take wing and show themselves off all around. Quite the contrary, the married ones in my tubes descend to the ultimate degree of humiliation.

Their predecessors, asexual, had wings, even while still enclosed within the gall, they sport on their plump rumps long streamers of ermine. For the sexual generation, the very flowers of the race; however, no wings, no snowy finery, no plump bright orange bellies. They are the most abject, weakest stage in the entire lineage. Sexuality, though progress everywhere else, is here decadence, it is a derision of the great law of living things.

Up till now, the aphid colonists of the terebinth have reproduced free from the constraints of bisexualism. Far from suffering from this, the species has prospered magnificently, so much so that, in a single season an individual reproduces itself a hundredfold, perhaps a thousandfold. Why not continue this way indefinitely, following the example of the garlic of our gardens, the reeds of Provence, the sugar cane and so many others? What need is there to employ two in order to obtain that which one can provide so successfully on its own?

The reason for this abrupt change in methods is the change in what is produced. Comparable to the trunk that surrounds itself with suckers, the preceeding generations bring forth live young into the world that are active at birth and insert their stylets in the sides of the gall. The humble matron of the sexual generation, however, is dedicated solely to the egg, a delicate home in which life must preserve itself in a latent condition for a whole year. We had the cuttings, now we have the seed.

In order to resist weather and time, and keep the spark of life dormant until a distant future, the egg as well as the seed requires the association of two forces, each of them more efficient when they unite their strengths. As far as the primary motivation behind this need is concerned, it will be wise for us to admit that we have no idea, and that most likely we will never know.

Meanwhile let us observe how the course of events turns out for the aphid. After mating, the male, the green colored one, grabs on to a small fiber of the wadding in the end of the tube, and later the same day or the next, he dries up into a small grain of dust. He is dead. His companion remains in place, motionless.

I wish to observe a little bit of what occurs inside her body. The microscope reveals to me, below the translucent epidermis, an elliptical, milky orb with fine granulations. This orb occupies nearly the entire inner volume of the animalcule. It is an infinitely tiny nebula in which, instead of a sun, an egg congeals and forms into existence. Nothing else is visible, no ovarian tubules, no embryonic eggs in chains like rosary beads that are typical of other insects.

Nearly all of the maternal substance breaks up, fuses and molds itself, following new laws. She was animate, she becomes inert and congeals into a seed in which the future lies dormant. She lived, and, still essentially the same, she will revive. It would be difficult indeed to find a finer example of the lofty alchemy that presides over the transmutations of life.

What will emerge from this crucible? For the moment, nothing, for there will be no oviposition. The entire animalcule has become an egg, a single egg that has the dried up integument of the animalcule for a shell; and this egg conserves the legs, head, thorax, abdomen, the epidermal segmentation of its progenitor. To all appearances, except for its inert state, it is the image of the small louse from whence it came.

Now the cycle completes itself and takes us back to where we started, to those enigmatic corpuscles that I collected from under the lichens on the terebinth and from the fissures in the cut stems. The wadding plug in my tubes contained two kinds, black ones and red ones, identical to those furnished to me directly by the bush.

Like seeds, awaiting the return of the favorable season for germination, they remain immobile for nearly a whole year. Produced in May, they may not hatch until the following April. Thus the unusual cycle begins all over, so complex that it took these lines to summarize it.

The animalcule that emerges from the egg causes the tip of a newly formed leaf to swell up into a little red pocket. Alone she gives birth here to a family that gradually disperses and goes forth, one by one, to form new galls elsewhere. Thus the primary artisan of the gall procreates collaborators who, when mature, become humpbacked sac carriers, and adorn themselves in red. These are the zealous multipliers of the tribe. Their numerous descendants are apterous, orange aphids that metamorphosize in September, becoming black and winged.

At this time the distended galls break open, and the alates fly off into the countryside, where each one disseminates its litter of six to eight immatures. The latter spend the harsh season underground, probably at the bases of certain species of grasses.

Winged female aphid

During the winter season the daughter generation from the galls may reproduce, but at a much reduced rate. Ultimately their progeny consists of alates which, similar to those of the fall, abandon their underground lair and return to the terebinth, on which they deposit the contents of their abdomens, again six to eight immatures, either in the fissures or under the cover of the lichens.

Until now, all of these aphids, out of diverse genealogical lineages, have given birth asexually; now the sexual stage appears and with it its end product, the egg. The progeny of the spring alates is a mixture of males and females, feeble creatures, the least among the whole series. These dwarfs, incapable of eating, mate, they have nothing else to do. Shortly afterwards the male perishes, the female; however, becomes immobile and passes on to the egg stage.