Part 2

The middle legs place a relatively small amount of pollen directly upon the pollen masses in the corbiculæ. This is accomplished when the brushes of the middle legs are used to pat down the pollen masses and to render them more compact. (See fig. 6.) The legs are used for this purpose quite often during the process of Loading the baskets, and a small amount of pollen is incidentally added to the masses when the brushes come into contact with them. A misinterpretation of this action has led some observers into the erroneous belief that all or nearly all of the corbicular pollen is scraped from the middle-leg brushes by the hairs which fringe the sides of the baskets. The middle legs do not scrape across the baskets, but merely pat downward upon the pollen which is there accumulating.

It is also possible that, in transferring pollen from the middle leg of one side to the planta of the opposite hind leg, the middle-leg brush may touch and rub over the pecten of the hind leg and thus directly place some of its pollen behind the pecten spines. Such a result is, however, very doubtful.

ACTION OF THE HIND LEGS.

The middle legs contribute the major portion of the pollen which reaches the hind legs, and all of it in cases where all of the pollen first reaches the bee in the region of the mouth. However, when much pollen falls upon the body of the bee the hind legs collect a little of it directly, for it falls upon their brushes and is collected upon them when these legs execute cleansing movements to remove it from the ventral surface and sides of the abdomen. All of the pollen which reaches the corbiculæ, with the exception of the small amount placed there by the middle legs when they pat down the pollen masses, passes first to the pollen combs of the plantæ.

When in the act of loading pollen from the plantar brushes to the corbiculæ the two hind legs hang beneath the abdomen with the tibio-femoral joints well drawn up toward the body. (See fig. 7.) The two plantæ lie close together with their inner surfaces nearly parallel to each other, but not quite, since they diverge slightly at their distal ends. The pollen combs of one leg are in contact with the pecten comb of the opposite leg. If pollen is to be transferred from the right planta to the left basket, the right planta is drawn upward in such a manner that the pollen combs of the right leg scrape over the pecten spines of the left. By this action some of the pollen is removed from the right plantar combs and is caught upon the outer surfaces of the pecten spines of the left leg.

This pollen now lies against the pecten and upon the flattened distal end of the left tibia. At this moment the planta of the left leg is flexed slightly, thus elevating the auricle and bringing the auricular surface into contact with the pollen which the pecten has just received. By this action the pollen is squeezed between the end of the tibia and the surface of the auricle and is forced upward against the distal end of the tibia and on outward into contact with the pollen mass accumulating in the corbicula. As this act, by which the left basket receives a small contribution of pollen, is being completed, the right leg is lowered and the pecten of this leg is brought into contact with the pollen combs of the left planta, over which they scrape as the left leg is raised, thus depositing pollen upon the lateral surfaces of the pecten spines of the right leg. (See fig. 7.)

Right and left baskets thus receive alternately successive contributions of pollen from the planta of the opposite leg. These loading movements are executed with great rapidity, the legs rising and falling with a pump-like motion. A very small amount of pollen is loaded at each stroke and many strokes are required to load the baskets completely.

If one attempts to obtain, from the literature of apiculture and zoology, a knowledge of the method by which the pollen baskets themselves are loaded, he is immediately confused by the diversity of the accounts available. The average textbook of zoology follows closely Cheshire's (1886) description in which he says that "the legs are crossed, and the metatarsus naturally scrapes its comb face on the upper edge of the opposite tibia in the direction from the base of the combs toward their tips. These upper hairs * * * are nearly straight, and pass between the comb teeth. The pollen, as removed, is caught by the bent-over hairs, and secured. Each scrape adds to the mass, until the face of the joint is more than covered, and the hairs just embrace the pellet." Franz (1906) states that (translated) "the final loading of the baskets is accomplished by the crossing over of the hind-tarsal segments, which rub and press upon each other." Many other observers and textbook writers evidently believed that the hind legs were crossed in the loading process.

On the other hand, it is believed by some that the middle legs are directly instrumental in filling the baskets. This method is indicated in the following quotation from Fleischmann and Zander (1910) (translated):

The second pair of legs transfer the pollen to the hind legs, where it is heaped up in the pollen masses. The tibia of each hind leg is depressed on its outer side, and upon the edges of this depression stand two rows of stiff hairs which are bent over the groove. The brushes of the middle pair of legs rub over these hairs, liberating the pollen, which drops into the baskets.

A suggestion of the true method is given by Hommell (1906), though his statements are somewhat indefinite. After describing the method by which pollen is collected, moistened, and passed to the middle legs he states that (translated) "the middle legs place their loads upon the pollen combs of the hind legs. There the sticky pollen is kneaded and is pushed across the pincher (_à traverse la pince_), is broken up into little masses and accumulates within the corbicula. In accomplishing this, the legs cross and it is the tarsus of the right leg which pushes the pollen across the pincher of the left, and reciprocally. The middle legs never function directly in loading the baskets, though from time to time their sensitive extremities touch the accumulated mass, for the sake of giving assurance of its position and size."

The recent valuable papers of Sladen (1911, 1912, _a_, _b_, _c_, _d_, and _e_), who was the first to present a true explanation of the function of the abdominal scent gland of the bee, give accounts of the process by which the pollen baskets are charged, which are in close accord with the writer's ideas on this subject. It is a pleasure to be able to confirm most of Sladen's observations and conclusions, and weight is added to the probable correctness of the two descriptions and interpretations of this process by the fact that the writer's studies and the conclusion based upon them were made prior to the appearance of Sladen's papers and quite independent of them. His description of the basket-loading process itself is so similar to the writer's own that a complete quotation from him is unnecessary. A few differences of opinion will, however, be noted while discussing some of the movements which the process involves. As will later be noted, our ideas regarding the question of pollen moistening, collecting, and transference are somewhat different.

ADDITIONAL DETAILS OF THE BASKET-LOADING PROCESS.

The point at which pollen enters the basket can best be determined by examining the corbiculæ of a bee shortly after it has reached a flower and before much pollen has been collected. Within each pollen basket of such a bee is found a small mass of pollen, which lies along the lower or distal margin of the basket. (See fig 8, _a_.) It is in this position because it has been scraped from the planta of the opposite leg by the pecten comb and has been pushed upward past the entrance of the basket by the continued addition of more from below, propelled by the successive strokes of the auricle. Closer examination of the region between the pecten and the floor of the basket itself shows more pollen, which is on its way to join that already squeezed into the basket.

If the collecting bee is watched for a few moments the increase will readily be noted and the fact will be established that the accumulating mass is gradually working upward or proximally from the lower or distal edge of the corbicula and is slowly covering the floor of this receptacle. (See figs. 8, _b_, _c_, and _d_.) In many instances the successive contributions remain for a time fairly separate, the whole mass being marked by furrows transverse to the long axis of the tibia.

Sladen (1912, _b_) notes the interesting fact that in those rather exceptional cases when a bee gathers pollen from more than one species of flowers the resulting mass within the corbicula will show a stratification parallel to the distal end, a condition which could result only from the method of loading here indicated.

As the pollen within the basket increases in amount it bulges outward, and projects downward below the lower edge of the basket. It is held in position by the long hairs which fringe the lateral sides of the basket, and its shape is largely determined by the form of these hairs and the direction in which they extend. When the basket is fully loaded the mass of pollen extends laterally on both sides of the tibia, but projects much farther on the posterior side, for on this side the bounding row of hairs extends outward, while on the anterior edge the hairs are more curved, folding upward and over the basket. As the mass increases in thickness by additions from below it is held in position by these long hairs which edge the basket. They are pushed outward and many of them become partly embedded in the pollen as it is pushed up from below. When the pollen grains are small and the whole mass is well moistened the marks made by some of the hairs will be seen on the sides of the load. (See fig. 9, _a_.) These scratches are also transverse in direction and they show that the mass has been increased by additions of pollen pushed up from below.

Even a superficial examination of a heavily laden basket shows the fallacy of the supposition that the long lateral fringing hairs are used to comb out the pollen from the brushes of either the hind or middle legs by the crossing of these legs over the lateral edges of the baskets. They are far from sufficiently stiff to serve this purpose, and their position with relation to the completed load shows conclusively that they could not be used in the final stages of the loading process, for the pollen mass has completely covered many of them and its outer surface extends far beyond their ends. They serve merely to hold the pollen in place and to allow the load to project beyond the margins of the tibia.

The auricle plays a very essential part in the process of loading the basket. This structure comprises the whole of the flattened proximal surface of the planta, except the joint of articulation itself, and it extends outward in a posterior direction a little beyond the remaining plantar edge. The surface of the auricle is covered over with many blunt, short spines and its lateral margin is bounded by a row of short rather pliable hairs, branched at their ends. When the planta is flexed the auricle is raised and its surface approaches the distal end of the tibia, its inner edge slipping up along the pecten spines and its outer hairy edge projecting into the opening which leads to the pollen basket. (See fig. 8, _b_.) With each upward stroke of the auricle small masses of pollen which have been scraped from the plantar combs by the pecten are caught and compressed between the spiny surface of the auricle and the surface of the tibia above it. The pressure thus exerted forces the pasty pollen outward and upward, since it can not escape past the base of the pecten, and directs it into the entrance to the corbicula. The outward and upward slant of the auricular surface and the projecting hairs with which the outer edge of the auricle is supplied also aid in directing the pollen toward the basket. Sladen (1911) states that in this movement the weak wing of the auricle is forced backward, and thus allows the escape of pollen toward the basket entrance, but this appears both doubtful and unnecessary, since the angle of inclination of the auricular surface gives the pollen a natural outlet in the proper direction.

If the corbicula already contains a considerable amount of pollen the contributions which are added to it at each stroke of the auricle come in contact with that already deposited and form a part of this mass, which increases in amount by continued additions from below. If, however, the corbicula is empty and the process of loading is just beginning, the first small bits of pollen which enter the basket must be retained upon the floor of the chamber until a sufficient amount has accumulated to allow the long overcurving hairs to offer it effective support. The sticky consistency of the pollen renders it likely to retain contact with the basket, and certain structures near the entrance give additional support. Several small sharp spines, seven or eight in number, spring from the floor of the basket immediately within the entrance, and the entire lower edge of the corbicula is fringed with very small hairs which are branched at their ends. (See fig. 3.) One large hair also springs from the floor of the basket, somewhat back from the entrance, which may aid in holding the pollen, but it can not function in this manner until a considerable amount has been collected.

As the pollen mass increases in size and hangs downward and backward over the pecten and auricle it shows upon its inner and lower surface a deep groove which runs outward from the entrance to the basket. (See fig. 9, _b_.) This groove results from the continued impact of the outer end of the auricle upon the pollen mass. At each upward stroke of the auricle its outer point comes in contact with the stored pollen as soon as the mass begins to bulge backward from the basket.

Although the process is a rather delicate one, it is entirely possible so to manipulate the hind legs of a recently killed bee that the corbiculæ of the two legs receive loads of pollen in a manner similar to that above described. To accomplish this successfully the operator must keep the combs of the plantæ well supplied with moistened pollen. If the foot of first one leg and then the other is grasped with forceps and so guided that the pollen combs of one leg rasp over the pecten spines of the other, the pollen from the combs will be transferred to the corbiculæ. To continue the loading process in a proper manner, it is also necessary to flex the planta of each leg just after the pollen combs of the opposite leg have deposited pollen behind the pecten. By this action the auricle is raised, compressing the pollen which the pecten has secured, and forcing some upward into the corbicula. Bees' legs which have been loaded in this artificial manner show pollen masses in their corbiculæ which are entirely similar in appearance to those formed by the labors of the living bee. Moreover, by the above method of manipulation the pollen appears first at the bottom of the basket, along its lower margin, gradually extends upward along the floor of the chamber, comes in contact with the overhanging hairs, and is shaped by them in a natural manner. All attempts to load the baskets by other movements, such as crossing the hind legs and scraping the plantar combs over the lateral edges of the baskets, give results which are entirely different from those achieved by the living bee.

POLLEN MOISTENING.

Many descriptions have been written by others of the method by which pollen is gathered and moistened. Some of these are indefinite, some are incorrect, while others are, in part, at least, similar to my own interpretation of this process. A few citations will here be given:

The bee first strokes the head and the proboscis with the brushes of the forelegs and moistens these brushes with a little honey from the proboscis, so that with later strokes all of the pollen from the head is collected upon these brushes. Then the middle-leg brushes remove this honey-moistened pollen from the forelegs and they also collect pollen from the breast and the sides of the thorax.--[Translation from Alefeld, 1861.]

In his account of the basket-loading process Alefeld assigns to the middle-leg brushes the function of assembling all of the pollen, even that from the plantar combs, and of placing it on the corbiculæ, this latter act being accomplished by combing over the hairy edge of each basket with the middle-leg brush of the same side.

It appears probable that the bee removes the pollen from the head, breast, and abdomen by means of the hairy brushes which are located upon the medial sides of the tarsal segments of all of the legs, being most pronounced upon the hind legs. The pollen is thus brought together and is carried forward to the mouth, where it is moistened with saliva and a little honey.--[Translation from Franz, 1906.]

Franz then says that this moistened pollen is passed backward and loaded.

Since the pollen of many plants is sticky and moist it adheres to the surface of the basket. Dry pollen is moistened by saliva, so that it also sticks,--[Translation from Fleischmann and Zander. 1910.]

Pollen is taken from flowers principally by means of the tongue, but at times, also, by the mandibles, by the forelegs, and middle legs. The brushes of the hind legs also load themselves, collecting from the hairs of the body. The pollen dust thus gathered is always transmitted to the mouth, where it is mixed with saliva.--[Translation from Hommell, 1906.]

Sladen considers the question of how pollen is moistened by the honey bee, humblebee (bumblebee), and some other bees, but does not appear to reach definite conclusions. In one of his papers (1912, _c_) he states that the pollen of some plants may be found in the mouth cavity and in the region of the mouth, but he reaches the conclusion that this pollen is comparatively "dry," using the word in a "relative sense." He asserts that "nowhere but on the corbicula and hind metatarsal brushes did I find the sticky pollen, except sometimes on the tips of the long, branched hairs on the back (upper) edges of the tibiæ and femora of the middle legs, and then only in heavily laden bees, where it is reasonable to suppose it had collected accidentally as the result of contact with the hind metatarsal brushes."

These and other considerations lead Sladen to think that, in the case of the bumblebee at least, the pollen "may be moistened on the hind metatarsus with the tongue." He states that the tongue of the bumblebee is of sufficient length to reach the hind metatarsus (planta) and that it might rub over the brushes of the metatarsi or be caught between them when they are approximated and thus moisten the two brushes simultaneously. However, he has never seen the tongue of the collecting honey bee brought near to the hind legs, and it appears probable to him that it can not easily reach them. "Possibly the middle or front legs are used as agents for conveying the honey" (in the case of the honey bee). "In the humblebee the tongue is longer, and it could more easily moisten the hind legs in the way suggested."

In an earlier paper Sladen (1912, _a_) gives the following as his opinion of the "way in which pollen dust is moistened with nectar," although he states that this is one of the points "which still remains obscure":

The only satisfactory manner in which, it seems to me, this can be done is for the tongue to lick the tarsi or metatarsi of the forelegs, which are covered with stiff bristles, well suited for holding the nectar, the nectar being then transferred to the metatarsal brushes on the middle legs, and from these, again, to the metatarsal brushes on the hind legs. The latter being thus rendered sticky, the pollen dust would cling to them. The different pairs of legs were certainly brought together occasionally, but not after every scrape of the hind metatarsi, and their movements were so quick that it was impossible to see what was done. Still, several pollen-collecting bees that I killed had the tarsi and metatarsi of the forelegs and the metatarsal brushes of the middle and hind legs moistened with nectar, and I think it probable that the moistening process, as outlined, is performed, as a rule, during the flight from flower to flower.

Sladen (1912, _c_) also considers the possibility that the fluid which moistens the pollen might be secreted through the comb at the end of the tibia, through the tibio-tarsal joint, or from the surface of the auricle, but finds no evidence of glandular openings in these regions. A suggestion of a similar nature, apparently unknown to Sladen, was made by Wolff (1873), who describes "sweat-glands" which, he claims, are located within the hind tibia and the planta, and which pour a secretion upon the surface of the corbicula and upon the upper end of the planta through many minute openings located at the bases of hairs, particularly those which arise from the lateral margins of the corbicula. Wolff is convinced that the fluid thus secreted is the essential cohesive material by which the grains of pollen are bound together to form the solid mass which fills each fully loaded basket. He noticed that the mouthparts are used to collect pollen, and that some of it is moistened with "honey" or "nectar," but he does not consider that the fluid thus supplied is sufficient to explain adequately the facility with which the collecting bee brings together the scattered grains of pollen and packs them away securely in the baskets. Wolff's description of the basket-loading process itself is strikingly similar to that advocated later by Cheshire.