Pollen Collection and the Corbiculae
By: Clarence Collison
Pollen is the main source of protein in a honey bee’s diet and the primary food for their brood (Brodschneider and Crailsheim, 2010). To collect and transport pollen, honey bees mix it with regurgitated nectar and form it into a pellet. They carry the pellet on their hind (metathoracic) legs in a structure called the corbicula, or pollen basket. Previous research has shown that a colony will collect 10-26 kg of pollen per year (Brodschneider and Crailsheim, 2010). While the weights of a honey bee’s pollen pellets vary with the time of day and with the species of pollen, the average pollen pellet weighs 7.9 mg (García-García et al., 2004), with the honey bee carrying two pollen pellets, one on each hind leg. This means that an average colony will annually embark on up to 1.6 million foraging trips to collect up to 3.2 million pollen pellets to support colony survival. The corbicula, which has an average surface area of 1.81 mm2 (Milne and Pries, 1984), is a slightly concave, hairless plate surrounded on both sides by long setae, or hairs, that curve inwards. The corbicular hairs are attached to nerves and some of them can detect their angle of displacement, which signals to the bee the pollen pellet’s size (Ford et al., 1981). In the process of forming the pollen pellet, the hairs, at least at the top of the corbicula, become embedded into the pellet. In addition to the outer hairs, there is also a single spindle hair located just above the pollen press, and previous studies have found that this hair plays some role in the maximum possible volume of the pellet (Hodges, 1967). When the honey bee has finished foraging, it returns to the hive and selects a cell in which to deposit its pollen pellets (Matherne et al., 2021).
The collection of pollen is greatly influenced by the needs of the colony. Provided there are adequate honey stores in the colony, with an increase in the amount of brood the proportion of foragers that collect pollen and the amount of pollen increases. Although brood of all stages stimulates pollen collection, the larval stage is particularly effective. The smell of brood alone and contact with bees tending the brood are each partly responsible for foragers collecting pollen, but individual foragers must have access to the brood if they are to receive maximum stimulation to collect pollen. Evidently, the larvae produce a pheromone that stimulates pollen collection. The amount of pollen collected is also influenced by the pollen stores present, and giving pollen to a colony diminishes pollen collection and increases nectar collection. Irrespective of the presence of brood, the queen also induces pollen collection (Free, 1977).
The hairs which cover the body and appendages of the bee are of the utmost importance in the process of pollen gathering. These hairs may be classified as 1) branched hairs and 2) unbranched hairs, the latter including both long, slender hairs and stiff, spinelike structures. Of these two classes, the branched hairs are the more numerous. They make up the hairy coat of the head, thorax and abdomen, with the exception of short sensory spines, as those found upon the antennae and perhaps elsewhere, and the stiff unbranched hairs which cover the surfaces of the compound eyes (Phillips, 1905). Branched hairs are also found upon the legs; more particularly upon the more proximal segments. A typical branched hair is composed of a long slender main axis from which spring numerous short lateral barbs. Grains of pollen are caught and held in the angles between the axis and the barbs and between the barbs of contiguous hairs. The hairy covering of the body and legs thus serves as a collecting surface upon which pollen grains are temporarily retained and from which they are later removed by the combing action of the brushes of the legs (Casteel, 1912b).
Hair spacing on the honey bee’s body is tuned to the particles they collect to facilitate particle suspension for easy removal, while the hair spacing on the grooming legs enables the effective transfer of particles from the body to the legs and determines the amount of pollen removed during each swipe. It was found that grooming behavior is unaffected by pollen type or initial pollen accumulation. The presence of pollenkitt, or the viscous fluid on the surface of pollen, plays an important role in pollen accumulation. Honey bees accumulated half as many pollen grains when the pollenkitt was removed (Amador et al., 2017).
The mouthparts of the bee are also essential to the proper collection of pollen. The mandibles are used to scrape over the anthers of flowers, and considerable pollen adheres to them and is later removed. The same is true of the maxillae and tongue. From the mouth comes the fluid by which the pollen grains are moistened. The legs of the worker bee are especially adapted for pollen gathering. Each leg bears a collecting brush, composed of stiff, un-branched hairs set closely together. These brushes are located upon the first or most proximal tarsal segment of the legs, known technically as the palmse of the forelegs and as the plantse of the middle and hind pair. The brush of the foreleg is elongated and of slight width, that of the middle leg broad and flat, while the brush upon the planta of the hind leg is the broadest of all and is also the most highly specialized. In addition to these well-marked brushes, the distal ends of the tibiae of the fore and middle legs bear many stiff hairs, which function as pollen collectors, and the distal tarsal joints of all legs bear similar structures. The tibia and the planta of the hind leg of the worker bee are greatly flattened (Figure 1). The outer surface of the tibia is marked by an elongated depression, deepest at its distal end, and bounded laterally by elevated margins. From the lateral boundaries of this depression spring many long hairs, some of which arch over the concave outer surface of the tibia and thus form a kind of receptacle or basket to which the name corbicula or pollen-basket is given. The lower or distal end of the tibia articulates at its anterior edge with the planta. The remaining portion of this end of the tibia is flattened and slightly concave, its surface sloping upward from the inner to the outer surface of the limb. Along the inner edge of this surface runs a row of short, stiff, backwardly directed spines, from 15-21 in number, which form the pecten or comb of the tibia. The lateral edge of this area forms the lower boundary of the corbicular depression and is marked by a row of very fine hairs which branch at their free ends. Immediately above these hairs, springing from the floor of the corbicula, seven or eight minute spines are found, and above them one long hair which reaches out over the lower edge of the basket. The broad, flat planta (metatarsus or proximal tarsal segment of the hind leg) is marked on its inner surface by several rows of stiff, distally directed spines which form the pollen combs. About 12 of these transverse rows may be distinguished, although some of them are not complete. The most distal row, which projects beyond the edge of the planta, is composed of very, strong, stiff spines which function in the removal of wax scales (Casteel, 1912a). The upper or proximal end of the planta is flattened and projects in a posterior direction to form the auricle. The surface of the auricle (pollen press) is marked with short, blunt spines, pyramidal in form and a fringe of fine hairs with branching ends extends along its lateral edge. This surface slopes upward and outward (Casteel, 1912b).
Figure 1. The honey bee workers hind leg, inner and outer
surfaces and details of the tibio-tarsal joint (auricle or pollen press). Dade, 1962.
After a bee has crawled over a few flowers, she begins to brush the pollen from her head, body and forward appendages and transfer it to the posterior pair of legs. This may be accomplished while she is resting on the flower, but more often while she hovers in the air before foraging for additional pollen. The wet pollen is removed from the mouthparts by the forelegs. The dry pollen clinging to the hairs of the head region also is removed by the forelegs, and added to the pollen moistened by the mouth (Gary, 1992).
The second pair of legs collects free pollen from the thorax, more particularly from the ventral region, and receives pollen collected by the first pair of legs. In taking pollen from the foreleg, the middle leg of the same side is extended forward and is either grasped by the flexed foreleg, or rubbed over it as the foreleg is bent downward and backward. Much sticky pollen is now assembled on the inner faces of the broad tarsal segments of the second pair of legs (Gary, 1992).
Pollen is transferred to the pollen baskets in at least two ways. A relatively small amount may reach the pollen baskets directly, as the middle legs sometimes are used to pat down the pollen accumulated there. But by far the larger amount is first transferred onto the pollen combs on the inner surfaces of the hind legs. One of the middle legs and then the other alternately is grasped between the first tarsal segments of the hind legs and drawn forward and upward, thus combing the pollen from the middle legs. The pollen now held in the combs of the hind basitarsus is next transferred to the pollen baskets on the outer surfaces of the hind tibiae (Gary, 1992).
With the two hind legs drawn up beneath the abdomen, the pollen combs of one leg are scraped by the pecten spines of the opposite one as the legs are moved up and down in a sort of pumping action (Figure 2). Thus, the pollen removed from one basitarsus is caught on the outside of the pecten comb of the opposite leg, the two combs scraping alternately. The planta is gently bent backward bringing its auricular surface into contact with the outer side of the pecten comb. By this action, the pollen mass is pushed along the slightly sloping lower end of the tibia and thence out onto the surface of the pollen basket at its lower end. Each new addition of pollen is pushed against the last and, simultaneously, the masses of pollen on both legs grow upward, a very small amount being added at each stroke (Figure 3) (Gary, 1992).
Figure 2. Pollen packing: the diagram shows a section through the pollen press. A) Press open, rastellum of right leg scrapping pollen out of the pollen combs of the left leg: pollen falls on auricle. B) Press closed, pollen forced through to outer side of right leg, where it is caught by the corbicula. Dade, 1962.
Figure 3. Pollen pellets forming on the corbicula (pollen basket). Transfer of pollen from the inner surface of the hind legs to the outer surface of the opposing hind leg. 1) The pollen rake scrapes pollen from the opposing combs and deposits it on the press. 2) Pollen is then pushed into the corbicula by pumping the legs and 3) transported back to the nest in a sticky ball moistened with regurgitated honey. Winston, 1987.
Finally, each leg is loaded with a mass of pollen, held in place by the long recurved hairs of the elevated margins of the tibiae. If the loads are very large, these hairs are pushed outward and become partly embedded in the pollen, allowing the mass to project beyond the margins of the tibiae. The bee accomplishes these brushing and combing actions so rapidly that the observer probably will fail to see some of the steps in the process without repeated observations (Gary, 1992).
When sensory hairs on the pollen basket signal that the load is completed, she returns to the hive. She may dance to recruit more foragers if the pollen source was very rewarding. Or she may immediately start moving around on the comb, especially in the areas immediately above the brood cells. Then, she sticks her head into the empty cells—one by one—and finally “selects” a cell in which to unload her pollen pellets. She grasps one edge of the cell with her forelegs and arches her abdomen so that its posterior end rests on the opposite side of the cell. Her hind legs are thrust inside the cell. She pries both pellets from the pollen baskets and they fall onto the lower cell wall. After a few cleaning movements she returns to foraging again. Despite elaborate cleaning behavior, large numbers of pollen grains remain on the bodies of pollen foragers after they unload the pellets (Gary, 2015).
House bees use their head and mandibles to tamp the pellets to the bottom of the cell into a compact mass. During this processing behavior, the bees often moisten the pellets with their mouthparts and add nectar or honey. The resulting pollen mass takes on a more moist appearance and becomes darker in color. Complex chemical reactions soon convert the pollen mass into a sticky, gummy consistency. Now it is called “bee bread”, a highly nutritious food eaten by nurse bees and ultimately converted into brood food fed to developing larvae (Gary, 2015).
The number of pollen foragers in a colony depends on the amount of larvae (brood) present at a given time, the quantity of stored pollen in the colony, individual forager genotype and available environmental resources (Pankiw et al., 1998). When pollen is artificially added to a colony, pollen foraging activity decreases until the excess pollen has been depleted through consumption. The quantity of stored pollen then returns to previous levels. When pollen is removed from a colony, the number of pollen foragers, their trip frequencies and their pollen load sizes increase until the amount of stored pollen is restored to the previous balance.
Fewell and Winston (1992) examined interactions between individual foraging behavior and pollen storage levels in the hive. Colonies responded to low pollen storage conditions by increasing pollen intake rates 54% relative to high pollen storage conditions, demonstrating a direct relationship between pollen storage levels and foraging effort. Approximately 80% of the difference in pollen intake rates was accounted for by variation in individual foraging effort, via changes in foraging activity and individual pollen load size. An additional 20% resulted from changes in the proportion of the foraging population collecting pollen. Under both high and low pollen storage treatments, colonies returned to pollen storage levels to pre-experimental levels within 16 days suggesting that honey bees regulate pollen storage levels around a homeostatic set point. They also found a direct relationship between pollen storage levels and colony brood production, demonstrating the potential for cumulative changes in individual foraging decisions to affect colony fitness.
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Clarence Collison is an Emeritus Professor of Entomology and Department Head Emeritus of Entomology and Plant Pathology at Mississippi State University, Mississippi State, MS.
