Place, the garden. Time, summer. Dramatis personae, a couple of small brown garden-ants, and a lazy clustering colony of wee green 'plant-lice,' or 'blight,' or aphides. The exact scene is usually on the young and succulent branches of a luxuriant rose-bush, into whose soft shoots the aphides have deeply buried their long trunk-like snouts, in search of the sap off which they live so contentedly through their brief lifetime. To them, enter the two small brown ants, their lawful possessors; for ants, too, though absolutely unrecognised by English law ('de minimis non curat lex,' says the legal aphorism), are nevertheless in their own commonwealth duly seised of many and various goods and chattels; and these same aphides, as everybody has heard, stand to them in pretty much the same position as cows stand to human herdsmen. Throw in for sole spectator a loitering naturalist, and you get the entire _mise-en-scene_ of a quaint little drama that works itself out a dozen times among the wilted rose-trees beneath the latticed cottage windows every summer morning.
It is a delightful sight to watch the two little lilliputian proprietors approaching and milking these their wee green motionless cattle. First of all, the ants quickly scent their way with protruded antennae (for they are as good as blind, poor things!) up the prickly stem of the rose-bush, guided, no doubt, by the faint perfume exhaled from the nectar above them. Smelling their road cautiously to the ends of the branches, they soon reach their own particular aphides, whose bodies they proceed gently to stroke with their outstretched feelers, and then stand by quietly for a moment in happy anticipation of the coming dinner. Presently, the obedient aphis, conscious of its lawful master's friendly presence, begins slowly to emit from two long horn-like tubes near the centre of its back a couple of limpid drops of a sticky pale yellow fluid. Honey-dew our English rustics still call it, because, when the aphides are not milked often enough by ants, they discharge it awkwardly of their own accord, and then it falls as a sweet clammy dew upon the grass beneath them. The ant, approaching the two tubes with cautious tenderness, removes the sweet drops without injuring in any way his little _protege_, and then passes on to the next in order of his tiny cattle, leaving the aphis apparently as much relieved by the process as a cow with a full hanging udder is relieved by the timely attention of the human milkmaid.
Evidently, this is a case of mutual accommodation in the political economy of the ants and aphides: a free interchange of services between the ant as consumer and the aphis as producer. Why the aphides should have acquired the curious necessity for getting rid of this sweet, sticky, and nutritious secretion nobody knows with certainty; but it is at least quite clear that the liquid is a considerable nuisance to them in their very sedentary and monotonous existence--a waste product of which they are anxious to disembarrass themselves as easily as possible--and that while they themselves stand to the ants in the relation of purveyors of food supply, the ants in return stand to them in the relation of scavengers, or contractors for the removal of useless accumulations.
Everybody knows the aphides well by sight, in one of their forms at least, the familiar rose aphis; but probably few people ever look at them closely and critically enough to observe how very beautiful and wonderful is the organisation of their tiny limbs in all its exquisite detail. If you pick off one good-sized wingless insect, however, from a blighted rose-leaf, and put him on a glass slide under a low power of the microscope, you will most likely be quite surprised to find what a lovely little creature it is that you have been poisoning wholesale all your life long with diluted tobacco-juice. His body is so transparent that you can see through it by transmitted light: a dainty glass globe, you would say, of emerald green, set upon six tapering, jointed, hairy legs, and provided in front with two large black eyes of many facets, and a pair of long and very flexible antennae, easily moved in any direction, but usually bent backward when the creature is at rest so as to reach nearly to his tail as he stands at ease upon his native rose-leaf. There are, however, two other features about him which specially attract attention, as being very characteristic of the aphides and their allies among all other insects. In the first place, his mouth is provided with a very long snout or proboscis, classically described as a rostrum, with which he pierces the outer skin of the rose-shoot where he lives, and sucks up incessantly its sweet juices. This organ is common to the aphis with all the other bugs and plant-lice. In the second place, he has half-way down his back (or a little more) a pair of very peculiar hollow organs, the honey tubes, from which exudes that singular secretion, the honey-dew. These tubes are not found in quite all species of aphides, but they are very common among the class, and they form by far the most conspicuous and interesting organs in all those aphides which do possess them.
The life-history of the rose-aphis, small and familiar as is the insect itself, forms one of the most marvellous and extraordinary chapters in all the fairy tales of modern science. Nobody need wonder why the blight attacks his roses so persistently when once he has learnt the unusual provision for exceptional fertility in the reproduction of these insect plagues. The whole story is too long to give at full length, but here is a brief recapitulation of a year's generations of common aphides.
In the spring, the eggs of last year's crop, which have been laid by the mothers in nooks and crannies out of reach of the frost, are quickened into life by the first return of warm weather, and hatch out their brood of insects. All this brood consists of imperfect females, without a single male among them; and they all fasten at once upon the young buds of their native bush, where they pass a sluggish and uneventful existence in sucking up the juice from the veins on the one hand, and secreting honey-dew upon the other. Four times they moult their skins, these moults being in some respects analogous to the metamorphosis of the caterpillar into chrysalis and butterfly. After the fourth moult, the young aphides attain maturity; and then they give origin, parthenogenetically, to a second brood, also of imperfect females, all produced without any fathers. This second brood brings forth in like manner a third generation, asexual, as before; and the same process is repeated without intermission as long as the warm weather lasts. In each case, the young simply bud out from the ovaries of the mothers, exactly as new crops of leaves bud out from the rose-branch on which they grow. Eleven generations have thus been observed to follow one another rapidly in a single summer; and indeed, by keeping the aphides in a warm room, one may even make them continue their reproduction in this purely vegetative fashion for as many as four years running. But as soon as the cold weather begins to set in, perfect male and female insects are produced by the last swarm of parthenogenetic mothers; and these true females, after being fertilised, lay the eggs which remain through the winter, and from which the next summer's broods have to begin afresh the wonderful cycle. Thus, only one generation of aphides, out of ten or eleven, consists of true males and females: all the rest are false females, producing young by a process of budding.
Setting aside for the present certain special modifications of this strange cycle which have been lately described by M. Jules Lichtenstein, let us consider for a moment what can be the origin and meaning of such an unusual and curious mode of reproduction.
The aphides are on the whole the most purely inactive and vegetative of all insects, unless indeed we except a few very debased and degraded parasites. They fasten themselves early in life on to a particular shoot of a particular plant; they drink in its juices, digest them, grow, and undergo their incomplete metamorphoses; they produce new generations with extraordinary rapidity; and they vegetate, in fact, almost as much as the plant itself upon which they are living. Their existence is duller than that of the very dullest cathedral city. They are thus essentially degenerate creatures: they have found the conditions of life too easy for them, and they have reverted to something so low and simple that they are almost plant-like in some of their habits and peculiarities.
The ancestors of the aphides were free winged insects; and, in certain stages of their existence, most living species of aphides possess at least some winged members. On the rose-bush, you can generally pick off a few such larger winged forms, side by side with the wee green wingless insects. But creatures which have taken to passing most of their life upon a single spot on a single plant hardly need the luxury of wings; and so, in nine cases out of ten, natural selection has dispensed with those needless encumbrances. Even the legs are comparatively little wanted by our modern aphides, which only require them to walk away in a stately sleepy manner when rudely disturbed by man, lady-birds, or other enemies; and indeed the legs are now very weak and feeble, and incapable of walking for more than a short distance at a time under exceptional provocation. The eyes remain, it is true; but only the big ones: the little ocelli at the top of the head, found amongst so many of their allies, are quite wanting in all the aphides. In short, the plant-lice have degenerated into mere mouths and sacks for sucking and storing food from the tissues of plants, provided with large honey-tubes for getting rid of the waste sugar.
Now, the greater the amount of food any animal gets, and the less the amount of expenditure it performs in muscular action, the greater will be the surplus it has left over for the purposes of reproduction. Eggs or young, in fact, represent the amount thus left over after all the wants of the body have been provided for. But in the rose-aphis the wants of the body, when once the insect has reached its full growth, are absolutely nothing; and it therefore then begins to bud out new generations in rapid succession as fast as ever it can produce them. This is strictly analogous to what we see every day taking place in all the plants around us. New leaves are produced one after another, as fast as material can be supplied for their nutrition, and each of these new leaves is known to be a separate individual, just as much as the individual aphis. At last, however, a time comes when the reproductive power of the plant begins to fail, and then it produces flowers, that is to say stamens (male) and pistils (female), whose union results in fertilisation and the subsequent outgrowth of fruit and seeds. Thus a year's cycle of the plant-lice exactly answers to the life-history of an ordinary annual. The eggs correspond to the seeds; the various generations of aphides budding out from one another by parthenogenesis correspond to the leaves budded out by one another throughout the summer; and the final brood of perfect males and females answers to the flower with its stamen and pistils, producing the seeds, as they produce the eggs, for setting up afresh the next year's cycle.
This consideration, I fancy, suggests to us the most probable explanation of the honey-tubes and honey-dew. Creatures that eat so much and reproduce so fast as the aphides are rapidly sucking up juices all the time from the plant on which they fasten, and converting most of the nutriment so absorbed into material for fresh generations. That is how they swarm so fast over all our shrubs and flowers. But if there is any one kind of material in their food in excess of their needs, they would naturally have to secrete it by a special organ developed or enlarged for the purpose. I don't mean that the organ would or could be developed all at once, by a sudden effort, but that as the habit of fixing themselves upon plants and sucking their juices grew from generation to generation with these descendants of originally winged insects, an organ for permitting the waste product to exude must necessarily have grown side by side with it. Sugar seems to have been such a waste product, contained in the juices of the plant to an extent beyond what the aphides could assimilate or use up in the production of new broods; and this sugar is therefore secreted by special organs, the honey-tubes. One can readily imagine that it may at first have escaped in small quantities, and that two pores on their last segment but two may have been gradually specialised into regular secreting organs, perhaps under the peculiar agency of the ants, who have regularly appropriated so many kinds of aphides as miniature milch cows.
So completely have some species of ants come to recognise their own proprietary interest in the persons of the aphides, that they provide them with fences and cow-sheds on the most approved human pattern. Sometimes they build up covered galleries to protect their tiny cattle; and these galleries lead from the nest to the place where the aphides are fixed, and completely enclose the little creatures from all chance of harm. If intruders try to attack the farmyard, the ants drive them away by biting and lacerating them. Sir John Lubbock, who has paid great attention to the mutual relations of ants and aphides, has even shown that various kinds of ants domesticate various species of aphis. The common brown garden-ant, one of the darkest skinned among our English races, 'devotes itself principally to aphides which frequent twigs and leaves'; especially, so far as I have myself observed, the bright green aphis of the rose, and the closely allied little black aphis of the broad bean. On the other hand a nearly related reddish ant pays attention chiefly to those aphides which live on the bark of trees, while the yellow meadow-ants, a far more subterranean species, keep flocks and herds of the like-minded aphides which feed upon the roots of herbs and grasses.
Sir John Lubbock, indeed, even suggests--and how the suggestion would have charmed 'Civilisation' Buckle!--that to this difference of food and habit the distinctive colours of the various species may very probably be due. The ground which he adduces for this ingenious idea is a capital example of the excellent use to which out-of-the-way evidence may be cleverly put by a competent evolutionary thinker. 'The Baltic amber,' he says, 'contains among the remains of many other insects a species of ant intermediate between our small brown garden-ants and the little yellow meadow-ants. This is possibly the stock from which these and other allied species are descended. One is tempted to suggest that the brown species which live so much in the open air, and climb up trees and bushes, have retained and even deepened their dark colour; while others, such as the yellow meadow-ant, which lives almost entirely below ground, have become much paler.' He might have added, as confirmatory evidence, the fact that the perfect winged males and females of the yellow species, which fly about freely during the brief honeymoon in the open air, are even darker in hue than the brown garden-ant. But how the light colour of the neuter workers gets transmitted through these dusky parents from one generation to another is part of that most insoluble crux of all evolutionary reasoning--the transmission of special qualities to neuters by parents who have never possessed them.
This last-mentioned yellow meadow-ant has carried the system of domestication further in all probability than any other species among its congeners. Not only do the yellow ants collect the root-feeding aphides in their own nests, and tend them as carefully as their own young, but they also gather and guard the eggs of the aphides, which, till they come to maturity, are of course quite useless. Sir John Lubbock found that his yellow ants carried the winter eggs of a species of aphis into their nest, and there took great care of them. In the spring, the eggs hatched out; and the ants actually carried the young aphides out of the nest again, and placed them on the leaves of a daisy growing in the immediate neighbourhood. They then built up a wall of earth over and round them. The aphides went on in their usual lazy fashion throughout the summer, and in October they laid another lot of eggs, precisely like those of the preceding autumn. This case, as the practised observer himself remarks, is an instance of prudence unexampled, perhaps, in the animal kingdom, outside man. 'The eggs are laid early in October on the food-plant of the insect. They are of no direct use to the ants; yet they are not left where they are laid, exposed to the severity of the weather and to innumerable dangers, but brought into their nests by the ants, and tended by them with the utmost care through the long winter months until the following March, when the young ones are brought out again and placed on the young shoots of the daisy.' Mr. White of Stonehouse has also noted an exactly similar instance of formican providence.
The connection between so many ants and so many species of the aphides being so close and intimate, it does not seem extravagant to suppose that the honey-tubes in their existing advanced form at least may be due to the deliberate selective action of these tiny insect-breeders. Indeed, when we consider that there are certain species of beetles which have never been found anywhere except in ants' nests, it appears highly probable that these domesticated forms have been produced by the ants themselves, exactly as the dog, the sheep, and the cow, in their existing types, have been produced by deliberate human selection. If this be so, then there is nothing very out-of-the-way in the idea that the ants have also produced the honey-tubes of aphides by their long selective action. It must be remembered that ants, in point of antiquity, date back, under one form or another, no doubt to a very remote period of geological time. Their immense variety of genera and species (over a thousand distinct kinds are known) show them to be a very ancient family, or else they would not have had time to be specially modified in such a wonderful multiformity of ways. Even as long ago as the time when the tertiary deposits of Oeningen and Radoboj were laid down, Dr. Heer of Zurich has shown that at least eighty-three distinct species of ants already existed; and the number that have left no trace behind is most probably far greater. Some of the beetles and woodlice which ants domesticate in their nests have been kept underground so long that they have become quite blind--that is to say, have ceased altogether to produce eyes, which would be of no use to them in their subterranean galleries; and one such blind beetle, known as Claviger, has even lost the power of feeding itself, and has to be fed by its masters from their own mandibles. Dr. Taschenberg enumerates 300 species of true ants'-nest insects, mostly beetles, in Germany alone; and M. Andre gives a list of 584 kinds, habitually found in association with ants in one country or another. Compared with these singular results of formican selection, the mere production or further development of the honey-tubes appears to be a very small matter.
But what good do the aphides themselves derive from the power of secreting honey-dew? For we know now that no animal or plant is ever provided with any organ or part merely for the benefit of another creature: the advantage must at least be mutual. Well, in the first place, it is likely that, in any case, the amount of sugary matter in the food of the aphides is quite in excess of their needs; they assimilate the nitrogenous material of the sap, and secrete its saccharine material as honey-dew. That, however, would hardly account for the development of special secretory ducts, like the honey-tubes, in which you can actually see the little drops of honey rolling, under the microscope. But the ants are useful allies to the aphides, in guarding them from another very dangerous type of insect. They are subject to the attacks of an ichneumon fly, which lays its eggs in them, meaning its larvae to feed upon their living bodies; and the ants watch over the aphides with the greatest vigilance, driving off the ichneumons whenever they approach their little _proteges_.
Many other insects besides ants, however, are fond of the sweet secretions of the aphides, and it is probable that the honey-dew thus acts to some extent as a preservative of the species, by diverting possible foes from the insects themselves, to the sugary liquid which they distil from their food-plants. Having more than enough and to spare for all their own needs, and the needs of their offspring, the plant-lice can afford to employ a little of their nutriment as a bribe to secure them from the attacks of possible enemies. Such compensatory bribes are common enough in the economy of nature. Thus our common English vetch secretes a little honey on the stipules or wing-like leaflets on the stem, and so distracts thieving ants from committing their depredations upon the nectaries in the flowers, which are intended for the attraction of the fertilising bees; and a South American acacia, as Mr. Belt has shown, bears hollow thorns and produces honey from a gland in each leaflet, in order to allure myriads of small ants which nest in the thorns, eat the honey, and repay the plant by driving away their leaf-cutting congeners. Indeed, as they sting violently, and issue forth in enormous swarms whenever the plant is attacked, they are even able to frighten off browsing cattle from their own peculiar acacia.
Aphides, then, are essentially degraded insects, which have become almost vegetative in their habits, and even in their mode of reproduction, but which still retain a few marks of their original descent from higher and more locomotive ancestors. Their wings, especially, are useful to the perfect forms in finding one another, and to the imperfect ones in migrating from one plant to its nearest neighbours, where they soon become the parents of fresh hordes in rapid succession. Hence various kinds of aphides are among the most dreaded plagues of agriculturists. The 'fly,' which Kentish farmers know so well on hops, is an aphis specialised for that particular bine; and, when once it appears in the gardens, it spreads with startling rapidity from one end of the long rows to the other. The phylloxera which has spoilt the French vineyards is a root-feeding form that attacks the vine, and kills or maims the plant terribly, by sucking the vital juices on their way up into the fresh-forming foliage. The 'American blight' on apple trees is yet another member of the same family, a wee creeping cottony creature that hides among the fissures of the bark, and drives its very long beak far down into the green sappy layer underlying the dead outer covering. In fact, almost all the best-known 'blights' and bladder-forming insects are aphides of one kind or another, affecting leaves, or stalks, or roots, or branches.
It is one of the most remarkable examples of the limitation of human powers that while we can easily exterminate large animals like the wolf and the bear in England, or the puma and the wolverine in the settled States of America, we should be so comparatively weak against the Colorado beetle or the fourteen-year locust, and so absolutely powerless against the hop-fly, the turnip-fly, and the phylloxera. The smaller and the more insignificant our enemy, viewed individually, the more difficult is he to cope with in the mass. All the elephants in the world could have been hunted down and annihilated, in all probability, with far less labour than has been expended upon one single little all but microscopic parasite in France alone. The enormous rapidity of reproduction in the family of aphides is the true cause of our helplessness before them. It has been calculated that a single aphis may during its own lifetime become the progenitor of 5,904,900,000 descendants. Each imperfect female produces about ninety young ones, and lives long enough to see its children's children to the fifth generation. Now, ninety multiplied by ninety four times over gives the number above stated. Of course, this makes no allowance for casualties which must be pretty frequent: but even so, the sum-total of aphides produced within a small garden in a single summer must be something very extraordinary.
It is curious, too, that aphides on the whole seem to escape the notice of insect-eating birds very tolerably. I cannot, in fact, discover that birds ever eat them, their chief real enemy being the little lizard-like larva of the lady-bird, which devours them everywhere greedily in immense numbers. Indeed, aphides form almost the sole food of the entire lady-bird tribe in their earlier stages of existence; and there is no better way of getting rid of blight on roses and other garden plants than to bring in a good boxful of these active and voracious little grubs from the fields and hedges. They will pounce upon the aphides forthwith as a cat pounces upon the mice in a well-stocked barn or farmyard. The two-spotted lady-bird in particular is the determined exterminator of the destructive hop-fly, and is much beloved accordingly by Kentish farmers. No doubt, one reason why birds do not readily see the aphis of the rose and most other species is because of their prevailing green tint, and the close way in which they stick to the leaves or shoots on whose juices they are preying. But in the case of many black and violet species, this protection of imitative colour is wanting, and yet the birds do not seem to care for the very conspicuous little insects on the broad bean, for example, whose dusky hue makes them quite noticeable in large masses. Here there may very likely be some special protection of nauseous taste in the aphides themselves (I will confess that I have not ventured to try the experiment in person), as in many other instances we know that conspicuously-coloured insects advertise their nastiness, as it were, to the birds by their own integuments, and so escape being eaten in mistake for any of their less protected relatives.
On the other hand, it seems pretty clear that certain plants have efficiently armed themselves against the aphides, in turn, by secreting bitter or otherwise unpleasant juices. So far as I can discover, the little plunderers seldom touch the pungent 'nasturtiums' or tropsaelums of our flower-gardens, even when these grow side by side with other plants on which the aphides are swarming. Often, indeed, I find winged forms upon the leaf-stem of a nasturtium, having come there evidently in hopes of starting a new colony; but usually in a dead or dying condition--the pungent juice seems to have poisoned them. So, too, spinach and lettuce may be covered with blight, while the bitter spurges, the woolly-leaved arabis, and the strong-scented thyme close by are utterly untouched. Plants seem to have acquired all these devices, such as close networks of hair upon the leaves, strong essences, bitter or pungent juices, and poisonous principles, mainly as deterrents for insect enemies, of which caterpillars and plant-lice are by far the most destructive. It would be unpardonable, of course, to write about honey-dew without mentioning tobacco; and I may add parenthetically that aphides are determined anti-tobacconists, nicotine, in fact, being a deadly poison to them. Smoking with tobacco, or sprinkling with tobacco-water, are familiar modes of getting rid of the unwelcome intruders in gardens. Doubtless this peculiar property of the tobacco plant has been developed as a prophylactic against insect enemies: and if so, we may perhaps owe the weed itself, as a smokable leaf, to the little aphides. Granting this hypothetical connection, the name of honey-dew would indeed be a peculiarly appropriate one. I may mention in passing that tobacco is quite fatal to almost all insects, a fact which I present gratuitously to the blowers of counterblasts, who are at liberty to make whatever use they choose of it. Quassia and aloes are also well-known preventives of fly or blight in gardens.
The most complete life-history yet given of any member of the aphis family is that which M. Jules Lichtenstein has worked out with so much care in the case of the phylloxera of the oak-tree. In April, the winter eggs of this species, laid in the bark of an oak, each hatch out a wingless imperfect female, which M. Lichtenstein calls the foundress. After moulting four times, the foundress produces, by parthenogenesis, a number of false eggs, which it fastens to the leaf-stalks and under side of the foliage. These false eggs hatch out a larval form, wingless, but bigger than any of the subsequent generations; and the larvae so produced themselves once more give origin to more larvae, which acquire wings, and fly away from the oak on which they were born to another of a different species in the same neighbourhood. There these larvae of the second crop once more lay false eggs, from which the third larval generation is developed. This brood is again wingless, and it proceeds at once to bud out several generations more, by internal gemmation, as long as the warm weather lasts. According to M. Lichtenstein, all previous observations have been made only on aphides of this third type; and he maintains that every species in the whole family really undergoes an analogous alternation of generations. At last, when the cold weather begins to set in, a fourth larval form appears, which soon obtains wings, and flies back to the same kind of oak on which the foundresses were first hatched out, all the intervening generations having passed their lives in sucking the juices of the other oak to which the second larval form migrated. The fourth type here produce perfect male and female insects, which are wingless, and have no sucking apparatus. The females, after being impregnated, lay a single egg each, which they hide in the bark, where it remains during the winter, till in spring it once more hatches out into a foundress, and the whole cycle begins over again. Whether all the aphides do or do not pass through corresponding stages is not yet quite certain. But Kentish farmers believe that the hop-fly migrates to hop-bines from plum-trees in the neighbourhood; and M. Lichtenstein considers that such migrations from one plant to another are quite normal in the family. We know, indeed, that many great plagues of our crops are thus propagated, sometimes among closely related plants, but sometimes also among the most widely separated species. For example, turnip-fly (which is not an aphis, but a small beetle) always begins its ravages (as Miss Ormerod has abundantly shown) upon a plot of charlock, and then spreads from patches of that weed to the neighbouring turnips, which are slightly diverse members of the same genus. But, on the other hand, it has long been well known that rust in wheat is specially connected with the presence of the barberry bush; and it has recently been proved that the fungus which produces the disease passes its early stages on the barberry leaves, and only migrates in later generations to the growing wheat. This last case brings even more prominently into light than ever the essential resemblance of the aphides to plant-parasites.
[The end]
Grant Allen's essay: Honey-Dew