II.—Instinctive Behaviour in Insects
Since instinctive behaviour is, by definition, independent of experience, and since the animals which act instinctively are also, in many cases, able to act intelligently, it is clear that, apart from hereditary variations, we must expect to find acquired modifications of instinct. As Huber said of bees, their instinctive procedure often indicates “a little dose of judgment.” It is, indeed, exceedingly difficult, as a matter of observation, to distinguish between hereditary variation and acquired modification. For the rôle played by these two factors in any given behaviour can only be determined if the whole life-history of the individual be known, and if there be opportunities for comparing it with the complete life-histories of other members of its race. And this is seldom possible.
These considerations must be borne in mind as we proceed to a brief study of some of the instinctive modes of behaviour in insects.
Dr. and Mrs. Peckham’s investigations on the instincts and habits of the solitary wasps have been described in a volume[30] worthy to be placed by the side of Fabre’s “Souvenirs.” Their descriptions seem to glow with the warm sunshine, and are redolent of the fresh air which afforded the conditions under which the observations were conducted. We can but regret that, in extracting from their bright pages some of the salient facts, the natural delicacy and grace of their treatment must be lost. For we can only give the dry skeleton which they have clothed with the flesh of lively detail. They enumerate the following primary modes of instinctive behaviour:—
1. Stinging.
2. Taking a particular kind of food.
3. Method of attacking and capturing prey.
4. Method of carrying prey.
5. Preparing nest, and then capturing prey, or the reverse.
6. The mode of taking prey into the nest.
7. The general style and locality of the nest.
8. The spinning or not spinning of a cocoon, and its specific form when one is made.
When the young Pelopœus emerges from the pupa-case and gnaws its way out of the mud cell, with limp and flaccid wings, it responds to a touch by well-directed movements of the abdomen with thrusts of the sting, as perfect as those of the adult. There is clearly no opportunity here for either instruction or experience to afford any intelligent guidance. Stinging is an instinctive act. And it is an act of which great use is made in the capture of prey which shall serve for food to the young—it has a biological end. But the wasps of different species do not have to learn by experience what prey to attack. It is by instinct, too, that they take their proper food-supply, one caterpillars, another spiders, a third flies or beetles. So deeply seated, indeed, is the hereditary preference, that no fly-robber ever takes spiders, nor will the capturer of spiders change to caterpillars or beetles. Some keep to a few species or genera, while Philanthus punctatus preys chiefly or entirely on bees of the genus Halictus.
Romanes[31] thought that the manner of stinging and paralyzing their prey might “be justly deemed the most remarkable instinct in the world.” Spiders, insects, and caterpillars are stung, he says, “in their chief nerve-centres, in consequence of which the victims are not killed outright, but rendered motionless; they are then conveyed to a burrow and, continuing to live in their paralyzed condition for several weeks, are then available as food for the larvæ when these are hatched. Of course the extraordinary fact which stands to be explained is that of the precise anatomical, not to say also physiological knowledge which appears to be displayed by the insect in stinging only the nerve-centres of its prey.” Eimer[32] thought that it “is absolutely impossible that the animal has arrived at its habit otherwise than by reflection upon the facts of experience.” “At the beginning,” he says, “she probably killed larvæ by stinging them anywhere, and then placed them in the cell. The bad results of this showed themselves; the larvæ putrified before they could serve as food for the larval wasps. In the mean time the mother wasp discovered that those larvæ which she had stung in particular parts of the body were motionless but still alive, and then she concluded that larvæ stung in this particular way could be kept for a longer time unchanged as living motionless food.”
Now, since these wasps, when they have stored their nests and laid an egg on one of the victims, close it up once and for all, and take no further interest in it or its contents, there seems no opportunity, at any rate in the existing state of matters, for the acquisition of that experience on which Eimer relied. But both his explanation and Romanes’s difficulty are based on the following assumptions: first, that the victims are instinctively or habitually stung in the chief nerve-centres; secondly, that when thus stung they are not killed but remain paralyzed for weeks; and thirdly, that the marvellously definite and delicate instinctive behaviour is in direct relation to the uniform result of prolonged paralysis and consequent preservation of the food in the fresh state. But Dr. Peckham’s careful observations and experiments show that, with the American wasps, the victims stored in the nests are quite as often dead as alive; that those which are only paralyzed live for a varying number of days, some more, some less; that wasp larvæ thrive just as well on dead victims, sometimes dried-up, sometimes undergoing decomposition, as on living and paralyzed prey; that the nerve-centres are not stung with the supposed uniformity; and that in some cases paralysis, in others death, follows when the victims are stung in parts far removed from any nerve-centre. “We believe,” he says, “that the primary purpose of the stinging is to overcome resistance, and to prevent the escape of the victims, and that incidentally some of them are killed and others are paralyzed.”
If, therefore, as will probably be shown to be the case, these conclusions are found to be generally true for this interesting group of insects, the mystery of “the precise anatomical, not to say also physiological knowledge which appears to be displayed” by these wasps turns out to be one of our own fabrication. It melts away in the light of fuller and more searching investigation.
Fig. 11.—Solitary Wasp stinging Caterpillar (after Peckham).
It must not be supposed, however, from what has been said, that the behaviour in the act of stinging is altogether indefinite. On the contrary, each species proceeds in a relatively definite manner with some variation or modification of method. Philanthus punctatus, for example, stings the bees, on which she preys, under the neck, and the thrust is at once fatal. Dr. Peckham further notes that he was only successful in getting the wasps to sting when they were hunting; those that had not yet begun to store the nests paid no attention to the bees. This is an example of that internal factor to which reference was made in the last section. Marchal observed that Cerceris ornata runs the end of her abdomen along the under surface of the thorax of the bee, and delivers her thrust at the division of the segments—that is, where the sting can enter. The action does not imply any physiological knowledge. In general she begins at the neck. Spiders are usually, but not always, stung on the ventral surface. To give but one more example, Dr. Peckham observed in three cases the procedure of Ammophila urnaria which preys on caterpillars, and often, after stinging, bites the neck in several places, this process being termed malaxation. In three observed captures, all the caterpillars being of the same species and alike in size, the thrusts were given on the ventral surface near the middle line, between the segments. In the first, seven stings were given at the extremities (there being thirteen segments), the middle segments being left untouched, and no malaxation was practised. In the second, seven stings were again given, but in the anterior and middle segments, followed by slight malaxation. In both these cases the first three thrusts were in definite order, behind the third, the second, and the first segments successively. In the case of the third caterpillar, only one thrust was given, between the third and fourth segments—that is to say, in the position of the first stab in the other cases,—and after this one thrust there was prolonged malaxation. Of fifteen stored caterpillars examined, some lived only three days, others a little longer, while a few showed signs of life at the end of a fortnight. In more than one instance the second of the two caterpillars stored in each nest died and became discoloured before the first one was entirely eaten. The larva under such circumstances ate it with good appetite, and then spun its cocoon as if nothing unpleasant had occurred.
Fig. 12.—Solitary Wasp dragging a Caterpillar to its Nest (after Peckham).
The mode of carrying their booty is in these wasps instinctive, and relatively uniform. Ammophila urnaria grasps the caterpillar, near the anterior end, in her mandibles, and carries or drags it beneath her legs, walking forwards. It is generally but not always with the ventral surface uppermost. Pompilus takes hold of her spider anywhere, but always drags it over the ground, walking backwards. Oxybelus clasps her fly with her hind legs; Bembex with the second pair. Each works after her own fashion in a way that is relatively uniform for each species.
The general style of the nest, its mode of construction, and its method of closure, are always performed, says Dr. Peckham, by each species in a similar manner, not indeed in circumstantial detail, but quite in the same way in a broad sense. Variation or modification is always present, but the tendency to depart from a nest of a given type is not excessive. Some dig in the ground curved tunnels, with or without one or more chambers. Others bore into decaying wood; others use straws, or make tunnels in bramble stems; while the mud-daubers build cells in which to store the food and lay the egg. This is sometimes deposited on the first, sometimes on the last, sometimes on some intermediate victim, but generally in much the same place and position. Ammophila, for instance, lays it on the side of the sixth or seventh segment—that is to say, in about the mid position.
Some species first capture their prey, and then make the nest in which it is to be entombed. Others first prepare the nest, and then carry or drag their prey to it—often from considerable distances—quite irrespective of what seems to us the more appropriate method of the two under the particular circumstances of the case. And the way in which the victim is dragged into the nest is similarly a matter of inheritance. Each way is characteristic of the species concerned, and would be an important part of any definition of the animal based upon its modes of behaviour. For example, a Sphex places her grasshopper just at the entrance of the nest, which she then enters herself before dragging in her prey by the antennæ. When the wasp was in the hole, Fabre moved the victim a little way off; the wasp came out, brought the grasshopper to the entrance as before, and went in a second time. This was repeated about forty times, each time with the same result, until the patience of the naturalist was exhausted, and the persistent wasp took her booty in after her appropriate fashion. She must place the grasshopper close to the opening; she must then descend and examine the nest, and, after that, must drag it down. Nothing less than the performance of these acts in a certain order satisfies her instinctive impulse.
In a private letter, from which he kindly allows me to quote, Dr. Peckham says: “We have recently made some experiments on this wasp (Sphex ichneumonea). First we allow her to carry in her prey undisturbed, to see how far she was faithful to the traditions of her ancestors, and to observe her normal methods. On the next day, when she had placed her grasshopper just at the opening of the nest, and while she was below, we drew it back to a little distance. She came out, and we both repeated our operations four times—she running down into the nest, always after getting the grasshopper into position, and we as regularly drawing it away. The fifth time she changed her plan, seized it by the head and backed into the nest with it. The next day, at the fourth trial, she straddled it and walked head first into the nest with it; and on the fourth day, at the eighth trial, she backed in with it as on the second day.” These interesting observations show that the wasp has sufficient intelligence to modify her procedure in accordance with an unwonted situation. The “consecutive necessity,” as it has been termed, has a potent influence, but is not absolute.
Fabre notes a case of similar consecutive necessity in the case of the mason bee, Chalicodoma. If while a bee is provisioning its nest with honey and pollen the structure be destroyed, she sometimes breaks open a completed cell, and, having done so, goes on bringing more provision, though the cell already contains a sufficient store of food; and only when she has completed the superfluous storing does she deposit her egg and seal up the cell. So, too, when the cell is removed in an early stage of construction, and another completed cell already partially stored is substituted, the bee, instead of simply adopting the new cell, goes on building until the cell is as much as one-third beyond the usual height; then, and not till then, does she proceed in due course to the next stage of the instinctive procedure, the provisioning of the cell.
From our general knowledge of animal nature, we should expect to find parasitic forms ready to take advantage of the material stored by such insects as the solitary wasps and the mason bees. It is said that Chalicodoma provides nourishment to the larvæ of some sixteen unbidden guests. A parasitic bee (Stelis nasuta) breaks open a closed cell, and, after depositing its eggs, seals it up again with mortar. Since her eggs and larvæ develop more rapidly than those of the mason bee, they are first served with the store of provision, while the rightful owner is done out of its inheritance. By a curious act, of what appears to us like retributive justice, these parasitic larvæ sometimes fall a prey to another parasite, also a hymenopterous insect named Monodontomerus, the larvæ of which prey on the young of both bees. Another genus of the same family, Leucopsis (Fig. 13, F), also succeeds in piercing with its ovipositor, at a suitable spot, the walls of the Chalicodoma cell, and suspends its curious hooked egg (Fig. 13, G) on the delicate cocoon within which the chrysalis lies. Fabre found in some cases as many as five of these parasitic eggs on a single cocoon. But he never found more than one larva in any cell that he examined. The following is an epitome of his conclusions and inferences. From the parasitic egg is hatched a minute arched grub, with relatively large head and mandibles, and provided with a number of bristles, which aid it in progression (Fig. 13, H). It does not, however, at once attack the bee larva, but makes a series of excursions, the object of which is to reach and destroy any other parasitic eggs. This was not actually observed, but the eggs were found to have been destroyed, and there was seemingly no other means of destruction under the conditions maintained. The larva, this done, changes its skin and takes on a new form, destitute of bristles, with a very small head and minute mandibles (Fig. 13, I). In this new form it attacks the Chalicodoma larva, making a very small incision, through which the juices of the host are transferred to the guest without further injury to the grub. It is interesting to note that, if the facts are accurately described and the inferences are correct, there are associated with two types of instinctive behaviour two distinct types of structure. The creature can have no conscious control over its structural development, and there is no ground for assuming that it has any control over its instinctive behaviour.
Fig. 13.—Insect Larvæ. A, B, of Sitaris; C, D, E, of Argyromœba; G, H, I, of Leucopsis; F, imago of Leucopsis (after Fabre).
The specialization of structure and of instinctive behaviour, in accordance with a definite sequence of life-conditions, is even more remarkable in another of the many parasites which Chalicodoma unwittingly labours to nourish. This time it is a fly (Argyromœba), which lays a minute egg on the outside of the cell. From this egg is hatched a slender threadlike worm, barely one-twentieth of an inch in length (Fig. 13, C). It has three pairs of longish bristles near the anterior end, and a single yet longer pair at the hinder extremity. These aid it in creeping over the wall of the cell. Its small head is armed with short, stiff bristles. For many days it wanders over the surface of the cell, inserting its bristly head into each minute cranny and crack. Throughout this long period it has never a bite nor sup. Probably many of them never succeed in finding a crevice by which they can effect an entrance, but those that do manage to wriggle in undergo a change, lose their bristles, and develop a minute suctorial mouth, through which the contents of the larva are absorbed into their swelling bodies (Fig. 13, D). When fully grown they are quite helpless, and unable to get out from the cell in which they are now imprisoned. For months they lie quiescent, but in the succeeding spring they pass into a pupal condition very different from that of most flies. The relatively large head is armed with strong spines; the middle region bears bristles directed backwards; the posterior end has short spines (Fig. 13, E). Fixing itself to the interior of the cell by the latter, it strikes with its armoured head repeated blows on the walls of its prison until a breach is at last made, and sufficiently enlarged to form a suitable exit. Then the pupa-skin bursts, and the imago insect emerges and flies off. At each stage of life there is the closest relation between structure and behaviour, and each is equally adapted to a biological end of which the creature has never had an opportunity of gaining any experience.
Exceedingly multifarious are the ways in which insects thus provide for the future of young they will never see. Antherophagus lives in flowers, and is believed to seize with its mandibles humble bees, which then unwittingly bear the parasitic beetle to the nests in which alone the larvæ have been found. The larvæ of our common oil-beetle (Meloë) are parasitic on the bee, Anthophora. It deposits its ten thousand eggs without observable discrimination; but the active young larva instinctively seizes and attaches itself to any hairy object. Thousands must go astray. They have been found on hairy beetles, flies, and bees of the wrong genus. Some, however, become thus attached to the one suitable species, and are conveyed by the Anthophora to her nest, where they promptly eat the egg she lays. It is not difficult to picture to one’s self how this incompletely evolved instinct might be further perfected by natural selection, through the survival of those females which laid their eggs in the haunts of the bee-host. And such an advance in instinctive behaviour is seen in another and rarer beetle—Sitaris. Her eggs are laid in August near the entrance to a nest of the Anthophora. In September they hatch to form larvæ, which hibernate in groups till the following spring. Then they become active (Fig. 13, A), and attach themselves to hairy objects. Being near the Anthophora nest, there is an increased chance of their fastening upon this bee. The chance is still far from good, for if this were so, we should not find that the Sitaris laid as many as two thousand eggs. Still, on these grounds, we may presume that its chance of survival is about five times as good as that of Meloë, which lays ten thousand eggs. The larva is said generally to attach itself to a male bee, which is hatched earlier than his mate, and to pass on to the female at the nuptial period; but in any case it eventually slips on to the egg that she lays. This forms the food of the larva during the remainder of this stage of its existence. It then moults and assumes a new form, capable of feeding on the honey (Fig. 13, B); and, after further changes, becomes a pupa, and then assumes the imago condition.
In these cases the advantage is wholly on the side of the parasite. But there are cases of close relationship between insects and flowering plants where the instinctive behaviour gives rise to reciprocal benefit. The Yucca is a genus of American Liliaceous plants, with large pale sweet-smelling flowers; and these are dependent for fertilization on the instinctive behaviour of a small straw-coloured moth of the genus Pronuba. Just when the Yucca plant blossoms in the summer, the moths emerge from their chrysalis cases. They mate; and the female then flies to a flower, collects a pellet of pollen from the anthers, proceeds to another flower, pierces the pistil with her sharp ovipositor, lays her eggs among the ovules, and finally darting to the stigma stuffs the pollen pellet into its funnel-shaped extremity (Fig. 14). If the flower be not thus fertilized the ovules do not develop; and if the ovules do not develop the grubs which are hatched from the moth’s eggs die of starvation. There are enough ovules to supply food to the grubs, and leave a balance to continue the race of Yuccas.
Fig. 14.—Yucca Flower and Moth.
Whether the female moth is attracted to the flower by sight or smell, we do not know. And whether the male finds the female, in the case of the Yucca moth, through scent, we are not in a position to state with certainty. It has, however, been shown that in certain moths[33] some odour emitted by the female is the attractive stimulus, affecting sense-organs situated on the antennæ of the male. To females confined in an opaque vessel over the mouth of which gauze was tied, the males came in numbers; but when a clear glass vessel was inverted, and sand was packed round the mouth, so as to prevent the escape of air from the interior, no males came, though the imprisoned females were clearly visible. If the antennæ of the males were either removed or coated with shellac the moths failed to notice the females even when close to them. In what way the intact male is made aware of the direction from which the scent comes, we do not know—possibly by differential stimulation in the antennæ, the moth instinctively turning in the direction of greater stimulation. It will be seen, therefore, that in the case of the behaviour of the Yucca moth—behaviour which is essential to the biological end of reproduction—there is much detail concerning which we are ignorant. But for our present purpose the important point to notice is that the procedure of the female cannot be due to imitation; nor can it be the outcome of individually acquired experience; for the method of procedure is not gradually learnt, but is carried out without apparent hesitation the first and only time the appropriate occasion presents itself. Not only does the moth take no heed of her grubs, but they are so placed that she could not in any case ascertain by observation that only if the ovules are fertilized do her offspring thrive. She cannot possibly know what effect the stuffing of the pollen on to the stigma exercises, or indeed whether it have any effect at all. And yet generation after generation these moths collect the pollen from the anthers and bear it to the stigma. Spence’s words “without knowledge of the end in view” are amply justified in this case, as in other cases of typically instinctive behaviour.