Popular Science Monthly/Volume 41/June 1892/The Yucca Moth and Yucca Pollination
| THE YUCCA MOTH AND YUCCA POLLINATION.[1] |
By C. V. RILEY, Ph. D.
THE common belief, based upon the theological assumption that all things upon this terrestrial sphere are for man's especial benefit, was, and perhaps yet is, that flowers were endowed with beauty and fragrance for our particular pleasure. Let us look somewhat more closely into this matter, and see what modern science has to say about it. Ever since Linnæus used the sexual characteristics of flowers in classification, and Erasmus Darwin sang of the loves of the plants, the philosophy of fertilization in the plant kingdom has been fairly apprehended. It has long been recognized that plants are divisible into homomorphic or self-fertilizable, and heteromorphic or cross-fertilizable species. All diclinous plants, or those having separate male and female flowers, belong to the latter category, which is further classifiable according to the means by which cross-fertilization is effected. One class (termed anemophilæ) depend almost entirely on the wind, and in these, of which our pines and other conifers, our poplars, willows, grasses, etc., are examples, the pollen or male element obtains in enormous quantities, is easily detached, and is generally produced early in spring, when winds prevail, and frequently before the development of the leaves, which would tend to impede its dispersion. The flower is inconspicuous and the stigma or female organ generally branched or hairy, so as to increase the chance of catching the wind-borne pollen. Water is an agency in the fertilization of a few plants, of which the singular Vallisneria is a striking illustration; while a few are aided by birds and higher animals; but by far the greater number are fertilized, or, more strictly speaking, pollinized, by insects.
The most casual observer of Nature must have appreciated, years ago, the fact that flowers are very important to insects, furnishing the essentials of life to those of several orders, and especially to the Hymenoptera (bees, wasps, etc.) and Lepidoptera (butterflies and moths) in the form either of pollen or nectar. But that insects could be of any especial benefit to plants has only come to be acknowledged and fully appreciated of late years. Toward the close of the last century Christian Konrad Sprengel published an important work—Das entdeckte Geheimniss der Natur—in which he maintained that the color, form, odor, secretions, and the general structure of flowers had reference to insects which are essential as pollinizers. The importance of insects as agents in cross-fertilization was scarcely appreciated, however, until the late Charles Darwin published the results of his researches on Primula, Linum, Lythrum, etc., and his elaborate work on the fertilization of orchids. The publication of these works gave to flowers a new significance and to their study almost as great an impulse as did his immortal Origin of Species to the general study of biology. Hooker, Bennett, Axell, Delpino,
Fig. 1.—Flower of Yucca aloifolia, showing stouter pistil and shorter style as compared with filamentosa.
Hildebrand, Hermann Müller, and others abroad, and Dr. Gray and Prof. William Trelease in this country, have followed up this subject; and no one can familiarize himself with the results of their studies without a keen sense—if not a conviction—that in the vast number of cases Sprengel's early statement holds strictly true. By these deeper insights into the significances of the floral world, and their harmonies with the insect world, we learn to understand why night-blooming flowers are usually white, even where their day-blooming allies are brightly colored, as in the case of Lychnis vespertina and L. diurna; or why the calyx, which is usually hidden and green, becomes bright when exposed, as in the berberry and larkspur. Many flowers are known to close or "sleep," and while most of them follow the animal world in taking this rest at night, yet there are marked exceptions. The dandelion goes to rest at 5 p. m. and wakes at 7 a. m., while the popular names of "four o'clock" and "John-go-to-bed-at-noon" sufficiently indicate the sleeping hours of Mirabilis and Tragopogon. Sir John Lubbock tritely asks, "What is the meaning of sleep in flowers, if it is not in reference to insects?" The closing during those hours when the particular insects needed for pollination are at rest, would protect the flower from spoliation by useless raiders. This belief is also strengthened by the fact that anemophilous flowers, or those fertilized by the wind, never sleep, and that flowers which attract insects by smell emit their odor at particular hours.
But the most interesting fact not commonly understood, that has now been very fully established by the most thorough researches, is, that a very large number of plants, even where the sexes are united in the same flower, absolutely depend on insect aid for pollination, and that the contrivances to induce cross-fertilization are infinite in diversity, while the modifications in structure which these insects have undergone the better to fit them to perform this service, are equally remarkable. Yet in most cases we have adaptation of the plant only, and except in a few instances, as, for instance, in that Madagascar orchid, Angrœcum sesquipedale, where the nectary is so deep that its nectar can be reached only by a moth (like Macrosila cluentius) with a very long tongue, our orchids are not dependent for pollination on any one Lepidopterous species, but may be aided by many which have tongues of sufficient length.
There are, in fact, few plants which are dependent on a single species for pollination. So far as I know, the yuccas furnish the 
Fig. 2.—Pronuba yuccasella: a, larva; b, ♀ moth with closed wing; c, ♀ moth with wings expanded—natural sue; d, side view of larval joint; e, head of larva, beneath; f, head of larva, above; g, thoracic leg of same; h, maxilla; i, mandible; j, spinneret and labial palpi; k, antenna—enlarged. only instance of this kind, for they actually depend on some particular species of little white moths belonging to the Tineina and to the genus Pronuba. The yuccas are a very interesting genus of lily-like plants, so familiar to every one in our public and private gardens that I need not say very much about them (Fig. 1). There are numerous species and even sub-genera, but they are all characterized by anthers not reaching anywhere near the stigma, so that fertilization unaided can take place only by the merest accident. In other words, the stigmatic tube is nowhere within reach of the stamens, and the pollen either remains attached to the open and withered anthers or falls and remains in different-sized lumps on the inside of the perianth, and can not be introduced into the stigmatic tube without artificial aid.
Our commoner garden yuccas, forms of filamentosa, depend on the commoner yucca moth, Pronuba yuccasella (Fig. 2, b, c), and so do all the different species found east of the Rocky Mountains, so far as we yet know. During the daytime we may, by knowing what and where to seek, often find this moth, either singly or in pairs, resting with folded wings within the half-closed flowers. It is then not only hidden from ordinary view, but well protected by the imitative color of the front wings with that of the flower, so that close scrutiny is necessary for its detection. If we visit the plant after
"... the garish day
Has sped on his wheels of light away,"
and when, with full-blown perianth, the yucca stands in all her queenly beauty, and sends forth her perfume more strongly upon the night air, we shall, with a little patience, meet with this same moth, flitting swiftly from flower to flower and from plant to 
Fig. 3.—Generic Characters of Pronuba yuccasella: a, side-view of head and neck of female denuded, showing how the collected load of pollen (1) is held by the tentacles (2); b, maxillary tentacle and palpus; c, an enlarged spine; d, palpus separated; e, scale from front wing; f, front leg; g, labial palpus; h, i, front and hind wings denuded; j, anal joint of female with ovipositor—all enlarged. plant—the dusky nature of the hind wings and of the under surface of the front wings almost completely offsetting and neutralizing, when in motion, the upper silvery whiteness of the latter, and thus still rendering the insect a little difficult of detection. It is principally the male which we thus see flying and, by the aid of a "bull's-eye," we shall find the female for the most part busily at work in the flowers. He, with relatively stronger wing-power, can afford to spend in the most pleasurable way the few brief days allotted to him; but she is charged with a double duty, and loses little time in its performance. As a part of the maternal task of continuing her race, she must act as foster-mother to the plant in order to insure a proper supply of food to her larvæ, which, as we shall presently see, feed on its seeds.
As preliminary to a better understanding of the habits of the female, it will be well to draw attention to those structural peculiarities which distinguish her from all other species of her order, and which so admirably fit her for the work she has to do. Fig. 3 gives some details of the head (a), and an important structure which more particularly characterizes her and interests us is the maxillary tentacle, shown with its palpus at b. She has a pair of these organs, which are prehensile and spinous, and it is chiefly by means of these that she is able to collect and hold a relatively large load of pollen for the purpose of pollination. Another organ which is characteristic is the ovipositor (Fig. 4, b, d), which 
Fig. 4.—Genital Characters of Pronuba yuccasella: a, tip of ♀ abdomen rendered somewhat transparent; b, basal joint of ovipositor; c, its sculpture; d, terminal joint of same; e, tip still more enlarged; f, genitalia ♂ from side; g, genitalia ♂ from above; h, undeveloped egg from ovary—enlarged. is delicate and extensile, being a combination of lance and saw, and admirably adapted for cleaving through the young fruit and then running the egg, which is long and filiform, into the ovarian cavity.
Though all the acts of the female are nocturnal, it is not at all difficult to follow them with a lantern, for, albeit ordinarily shy, she may be closely approached when she is about to oviposit. Her activity begins soon after dark, but consists at first in assiduously collecting a load of pollen. She may be seen running up to the top of one of the stamens, and bending her head down over the anther, stretching the maxillary tentacles, so wonderfully modified for the purpose, to their fullest extent, the tongue uncoiled and reaching to the opposite side of the stamen (Fig. 6). In this manner she is able to obtain a firm hold of the same while the head is kept close to the anthers and moved peculiarly 
Fig. 5.—Pronuba yuccasella: l, male; m, female chrysalis—hair-line showing natural size. back and forth, something as in the motion of the head of a caterpillar when feeding. The maxillary palpi are used in this act very much as the ordinary mandibles are used in other insects, removing or scraping the pollen from the anthers toward the tentacles. After thus gathering the pollen, she raises her head and commences to shape it into a little mass or pellet by using her front legs very much as a cat does when cleansing her mouth, sometimes using only one leg, at another time both, smoothing and pressing the gathered pollen, the tentacles meanwhile stretching and curving. After collecting all the pollen from one anther, she proceeds to another and repeats the operation, then to a third and fourth, after which, with her relatively large load—often thrice as large as the head—held firmly against the neck and front trochanters, she usually runs about or flies to another plant: for I have often noticed that oviposition, as a rule, is accomplished in some other flower than that from which the pollen was gathered, and that cross-fertilization is thus secured.
Once fully equipped with this important commodity, she may be seen either crawling over or resting within the flower, generally 
Fig. 6.—Pronuba yuccasella, female, in the act of gathering pollen from the anthers; five times enlarged. with the head toward the base. From time to time she makes a sudden dart and deftly runs around the stamens, and anon takes a position with the body between and the legs straddling two of them, her head being usually turned toward the stigma. As the terminal halves of the stamens are always more or less recurved, she generally has to retreat between two of them until the tip of her abdomen can reach the pistil (Fig. 7). As soon as a favorable point is reached—generally just below the middle—she rests motionless for a short time, when the abdomen is slightly raised and the lance-like ovipositor is thrust into the soft tissue, held there the best part of a minute, while the egg is conducted to its destination, and then withdrawn by a series of up-and-down motions. Fig. 8 is a transverse section of the young fruit at this stage of the growth, indicating the manner in which it is punctured at a, a, and how the egg is conveyed into the ovarian cell at b, while Fig. 9 shows a longitudinal section of the pistil at a, the puncture of the ovipositor at b, and the egg within the ovarian cell at c.
The stigmatic liquor is not nectarian, and the flower secretes but a small amount of nectar at the base of the petals; and while these facts serve to disprove any positive value of their nectar in the pollination of the yucca flowers, they add to the importance of Pronuba by showing that the acts of collecting pollen and transferring it to the stigma do not result in any food compensation, as I was at first inclined to suppose. In other words, there is no nectar to allure other nectar-loving insects and cause them to go to the stigma; but, on the contrary, those which are drawn to the plant by the slight amount of nectar are led in the very opposite direction, viz., to the base of the style or of the flower. It is also an interesting fact that I have never noticed Pronuba feeding, as contradistinguished from pollinizing, for the motions of the tongue of Lepidoptera when feeding are quite characteristic and easily recognized. Indeed, the two pieces which form the tongue are so often separated at tip, and so weakly joined throughout, as to raise the question, in connection with a somewhat imperfect alimentary canal, as to whether the moth feeds at all, and to suggest that the rather strong tongue, otherwise, assists pollination.
No sooner is the ovipositor withdrawn into the abdomen than the moth runs up to the top of the pistil, thrusts the pollen into the stigmatic opening, and works her head rapidly—the motion
Fig. 7.—Flower of Yucca, with near petals removed to show normal position of Pronuba in ovipositing.
being mostly up and down and lasting several seconds. She works with a vigor that would indicate combined pleasure and purpose, and makes every effort to force the pollen into the tube, thrusting it ordinarily from the base of one of the three primary clefts of the style. After the more vigorous motions of thrusting the pollen into the tube, she frequently rests in comparative quiet, working her tongue in the tube sometimes for four or five minutes together, but ordinarily the act of pollination ceases with the few vigorous thrusts already described. The importance of this act will be better appreciated when I state that numerous experiments in artificial or brush pollination have shown that effective fertilization in Yucca filamentosa is by no means an easy matter, and that it rarely takes place as effectively as through the actions of Pronuba.
This carrying of the pollen to the stigma generally follows every act of oviposition, so that where ten or a dozen eggs are consigned to a single pistil, the stigma will be so many times bepollened.
The egg of Pronuba is an extremely delicate, thread-like structure, averaging 1·5 millimetre in length and less than 0·1 millimetre (Fig. 9, c) in diameter, tapering at the base and enlarging slightly toward the capitate end, which has also a slightly indurated point. It is impossible to follow it with the unaided eye, or in fact with an ordinary lens, even if the pistil be at once plucked and dissected; but, by means of careful microscopical sections, we may trace its course, as shown in Figs. 8 and 9.
The larva hatches in about a week and will be found at a point from eight to ten ovules above or below the external puncture, according as the egg was thrust above or below it. It has no pro-legs, but has well-developed thoracic legs. It matures with the ripening of the seeds, which differs in time in the different species of yucca, and also in the same species, but occupies on an average about a month in the ordinary Yucca filamentosa. The number of seeds destroyed is rarely more than a dozen and more frequently less, and I have recorded the fact of having found as
8.—Transverse Section of Pistil, about middle, one day after oviposition, showing (a, a) puncture of ovipositor, and (b, b) position of egg.
many as twenty-one larvae in a single pod. Just about the time the pods are hardening and ready to dehisce and the seeds have already colored, the full-grown larva bores its way out of the pod and makes its way to the ground. It remains as a larva within its cocoon during the fall, winter, and spring months, and only transforms to the chrysalis state a few days before the blooming of the yuccas. The chrysalis (Fig. 4), as shown in the figure, is armed with an acute spine on the head and with singular spatulate spines on the back, which are well fitted to enable it to work its way to the surface from its underground retreat.
The effect of the puncture of the female moth in oviposition is at once noticeable on the young fruit by a darker green discoloration externally. In time this becomes a depression, and the irregularities of the pods (Fig. 9, d, e; Fig. 10, b, c) which have been considered characteristic of the fruit of the genus are chiefly due to these punctures, which, ordinarily occurring just below the middle of the pod, produce a more or less marked constriction there.
Fig. 9.—a, longitudinal section of pistil of Yucca filamentosa, showing (b, b) punctures of Pronuba, and (c, c) the normal position of her eggs in the ovarian cell; d, section of a punctured carpel seven days after oviposition, showing the egg yet unhatched and the manner in which the ovules in the neighborhood of puncture have been arrested in development so as to cause the constriction; e, section of an older carpel, showing the larva above the original puncture; f, a seed thirteen days from oviposition, showing young larva at funicular base.
This I have often proved by artificially pollinizing the flowers and protecting them from Pronuba, when the pods will develop in a regular, parallel-sided manner (Fig. 10, a).
It is noticeable that all the pods do not contain Pronuba larvæ, though we rarely find any on the filamentose species that do not show the marks of puncture, which indicates that a great many punctures are fruitless in result, owing either to the difficulty of the operation of oviposition, or to the fact that the eggs, having been once consigned to the pistil, have failed to hatch, for one reason or another; or again, that the larva has, for one reason or another, perished. A similar mortality is connected with the similarly difficult and complicated oviposition of the Cynipidæ, as Adler has shown. In dissecting the young fruits of the filamentose yuccas, with a view to critical examination, I have found that about half of them, on the average, contain nothing; but the proportion varies greatly in different localities and according to circumstances, and I may say that, as a result of my numerous examinations, fully two thirds of the mature pods are found to contain the larvae of Pronuba. All the experiments which I have so far made, or have known to be made, prove conclusively that the capsular species never set fruit without her aid.
Pronuba yuccasella is found in all parts of the country east of the Rocky Mountains where the filamentose yuccas normally range; but has not extended to all sections where they are cultivated. The time of its appearance is strikingly coetaneous, east
Fig. 10.—Mature Pods of Yucca angustifolia: a, artificially pollinized and protected from Pronuba; b, normal pod, showing constrictions resulting from Pronuba puncture and exit-holes of larva; c, one of the lobes cut open, showing larva within.
of the Mississippi, with the blooming of filamentosa; while other cultivated species which bloom either earlier or later, and which, therefore, do not receive the visits of the moth, I have, as already stated, never known to bear seed. On the Western plains, where Y. angustifolia is native, the moth's season of appearance is adapted to the flowering of this particular yucca. In California, Yucca whipplei is pollinized by Pronuba maculata, an invariably maculate species; while, on the Mojave Desert, Yucca brevifolia is pollinized by Pronuba synthetica, a species still more abnormal than yuccasella and modified to fit it to the peculiarities of that particular species of yucca. In the Gulf States the typical yuccasella occurs, and fertilizes not only the filamentose yuccas, but those individuals of the larger, fleshy-fruited species like aloifolia which happen to bloom about the same time of the year.
Thus we find that some species of Pronuba is connected with all the yuccas so far studied in this connection, and I have no doubt that this will be found to be generally true, so far as the indigenous species are concerned, and that in the native home of any of the species we shall find that pollination depends upon some species of Pronuba. This is rendered certain by the fact that, wherever I have been able to examine the mature or partially mature fruit of other yuccas in herbaria, I have in almost every instance observed the constriction and in most instances seen traces of the puncture and the work of the larva.
We have, in the structures and functions which are so characteristic of this yucca moth, admirable adaptations of means to an end, whether for pollinizing the plant or providing for a future generation. The Pronuba larva rarely destroys more than a dozen of the seeds, so that several may develop within a single pod and yet leave many perfect seeds, while, for the reasons already stated, we occasionally have pods without a trace of the insect.
There is between Pronuba and its food-plant a mutual interdependence which excites our wonder, and is fraught with interesting suggestions to those who are in the habit of reasoning from effect to cause. Whether we believe, as I certainly do, that this perfect adaptation and adjustment have been brought about by slow degrees through the long course of ages, or whether we believe that they were always so from the beginning, they are equally suggestive. The peculiar structure of the flower which prevents self-fertilization, though on a superficial view it strike one as a disadvantage, is, in reality, of benefit, as the value of cross-fertilization has been fully established; while the maxillary tentacles of the female moth are very plainly an advantage to her species in the "struggle for life"; and it is quite easy to conceive, on Darwinian grounds, how both these characteristics have been produced in the course of time from archetypal forms which possessed neither, and in reality we get a good insight into the process in studying the characteristics of other species of the family Prodoxidæ. These peculiarities are, moreover, mutually and reciprocally beneficial, so that the plant and the animal are each influenced and modified by the other, and the same laws which produced the beneficial specialization of parts will maintain them by the elimination of all tendencies to depart from them.
The pollen grains would not adhere by chance to the rolled-up tentacles, and we have seen how full of apparent purpose and deliberation Pronuba's actions are, It may be that all her actions are the result merely of "blind instinct," by which term proud man has been wont to designate the doings of inferior animals; but no one can watch her operations without feeling that there is in all of them as much of purpose as there is in those of the female Pelopæus who so assiduously collects, paralyzes, and stores away in her mud-dabs the spiders which are to nourish her young; or in the many other curious provisions which insects make for their progeny, which, in the majority of instances, they are destined never to behold. Nor can I see any good reason for denying these lowly creatures a degree of consciousness of what they are about, or even of what will result from their labors. They have an object in view, and whether we attribute their performances to instinct or to reason depends altogether on the meaning we give to those words. Define instinct as "congenital habit" or "inherited association" or, as I prefer to characterize it, as the inevitable outcome of organization, and most of the doings of the lower animals may justly be called instinctive; but instinct and intelligence are both present, in most animals, in varying proportion, the last being called into play more especially by unusual and exceptional circumstances, and the power which guides the female Pronuba in her actions differs only in degree from that which directs a bird in the building of its nest, or which governs many of the actions of rational men.
- ↑ Adapted from advance sheets of the Annual Report of the Missouri Botanical Garden for 1891.