What takes the pollen

The bee hangs head-up from a spray of goldenrod florets. Both hind tibiae carry a smooth orange mass: the corbicular pollen load. It is not in a pouch or a cup. It sits on the flat outer face of the tibia, threaded through by the hairs that rim the basket.

Only females of the corbiculate tribes, the honey bees, bumblebees, stingless bees and orchid bees, have this apparatus.73 Male bumblebees have slender, hairy hind tibiae with no basket, and the females of the cuckoo bumblebees (subgenus Psithyrus), which do not provision nests of their own, lack the pollen-collecting apparatus too.74 The loaded baskets settle the sex of this bee: it is a female.

Whether it is a worker or a queen cannot be read from the picture. Queens collect pollen as well, above all when founding a nest in spring.64 Given the late season and the task, a worker is the likelier reading. The pale thoracic pile and the black abdomen with a pale first tergite fit the common eastern bumblebee, Bombus impatiens, and the angle does not confirm the species. The photograph shows the flower being visited; it does not show that the whole load came from goldenrod.

A bumblebee is covered in branched setae, and the branching comes in more than one form. A morphological survey of B. impatiens separates long-branched plumose hairs from short-branched spinulate hairs and maps where each kind sits on the body.79 Both kinds trap pollen grains in a way an unbranched hair cannot. When the bee pushes into a goldenrod head, the anthers of the disc florets dust its face, tongue, legs and underside with grains.

Three things make the grains stay. Contact, and the hooking of a spiny exine into branched hairs, do most of the work.71 The grains of goldenrod, like most Asteraceae, are coated in pollenkitt, an oily layer that sticks to whatever it touches; in the honey bee the hairs and the pollenkitt together account for capture and removal.76 Electrical forces can help as well: a flying bee accumulates charge, and a charged bee approaching a flower can induce an opposite charge on loose pollen so that grains are drawn to it.70 Pollen does not simply arrive negatively charged; airborne grains have been measured with either polarity,72 and no jumping distance has been measured for goldenrod and bumblebees.

The fringe that rims the corbicula is not uniform either. In B. impatiens it includes simple hairs and hairs with short branches on one side only, and those branches generally face away from the load.79 At the entrance of the basket, its distal end near the rastellum, a bumblebee carries two or three stout hairs; the honey bee has a single hair in the middle of the basket instead.68 The comb bristles and rake spines on the basitarsus and tibial apex are short and stout and do the mechanical work of moving pollen from one leg to the other.

Dry pollen does not pack. Between flowers the bee brings its forelegs up to its mouthparts and wets them with a droplet regurgitated from the crop. The crop, or honey stomach, is an expandable sac in the front of the abdomen where nectar is held before it is passed to the nest; it is drawn dashed in the first figure. The regurgitated fluid is nectar, sometimes nectar already concentrated toward honey, and its dissolved sugar is what makes the packing fluid viscous and tacky. Sladen described this wetting in bumblebees and Casteel in the honey bee, both in 1912.6465

Honey bee-collected pollen carries enzymes of glandular origin that anther pollen does not, one reason corbicular pollen differs chemically from pollen taken straight from the flower.75 That finding does not say which gland the enzymes came from, when they were added, or whether the same thing happens in bumblebees. The labial glands open at the base of the proboscis, so a salivary share in the packing fluid is plausible. No study has traced one in a bumblebee.

A bumblebee’s corbicular load is smooth, glossy and rounded because it is a paste, not a heap. Some bees that collect dry pollen, the species with a scopa rather than a corbicula, carry it loose in dense hair.68 The corbiculate bees traded most of that hair for a bare plate, a fringe and a moistened mass.

The mandibles bite anthers open on some flowers and, on the forelegs, help work the moistened pollen into a mass. The proboscis is a sheath of maxillary galeae and labial palpi around the glossa, the tongue; it delivers the regurgitated droplet and takes up nectar in the first place.67

The foreleg basitarsus carries a dense brush on its inner face. With it the bee sweeps pollen from the head, eyes, mouthparts and the front of the thorax. The same segment has a semicircular notch lined with a fine comb: the strigil, or antenna cleaner. A flattened spur on the tibia, the fibula, closes the notch so an antenna drawn through it is scraped clean on both sides.67 Pollen from the antennae enters the stream here.

The midleg basitarsus is also brushed. The midlegs strip the pollen off the forelegs and off the thorax, then hand it to the hind legs: the hind basitarsal combs scrape the midlegs as the legs are rubbed together. Later the midlegs pat and shape the growing loads.6569 In the nest the middle legs, chiefly their basitarsi, push the finished pellets off the corbiculae. Casteel saw the basitarsus do this in the honey bee and left the tibial spur’s part in it open.65

Everything that makes a pollen basket is on the last two big segments of the hind leg, the tibia and the basitarsus, and the joint between them. The fourth figure draws the whole leg small and those two segments large, from both faces.

The hind tibia is widened toward its apex and flattened. Its outer face is the corbicula, the pollen basket: a smooth, slightly concave, nearly bare plate, glossy where the surrounding cuticle is hairy.68 Both margins of the plate carry a fringe of long, stiff, curved setae that lean in over the floor; some are simple and some carry short one-sided branches facing outward.79 At the entrance of the basket, the distal end just above the rastellum, stand two or three stout hairs.68 The honey bee differs here: its basket has one hair, in the middle of the floor. The first pollen pressed into the basket meets the entrance hairs, and as the load grows the fringe hairs run into it from both sides.

The distal margin of the tibia carries the rastellum, a comb of short, stout spines that points toward the basitarsus. On its inner apical corner the bumblebee tibia has two spurs; the honey bee tibia has none, one of the easy ways to tell the two genera by the hind leg alone.73

The basitarsus is the first and much the largest tarsal segment, a broad flat plate hinged to the apex of the tibia at the tibio-basitarsal joint. The hinge is at the anterior corner, so when the joint flexes the posterior part of the basitarsus swings up toward the underside of the tibial apex. At that posterior basal corner the basitarsus carries a small projecting flange with a fringed edge: the auricle. The auricle and the rastellum face each other across the joint. Together they are the pollen press.6566

The inner face of the basitarsus bears the basitarsal combs, or brush: transverse rows of stiff bristles. This is the surface that collects pollen from the midlegs and the abdomen, and it is the surface the other hind leg’s rastellum rakes.65

The load is built from the bottom up, usually while the bee hovers or hangs between flowers. Each cycle moves a small mass of moist pollen from the brush of one hind leg onto the basket of the other, and every cycle enters the basket at the same place: the base of the corbicular surface, just above the rastellum. Sladen described the mechanism in bumblebees and Casteel published a detailed account for the honey bee the same year; Hodges drew it in 1952.646566

Rake. The hind legs are rubbed against each other. The rastellum on the distal margin of one tibia drags downward across the basitarsal combs of the opposite leg, stripping pollen out of the brush.65

Collect. The raked pollen is scraped into the press region of the raking leg: the gap between its own rastellum, above, and its own auricle, below. The transfer is driven by the scraping stroke, not by gravity.65

Press. The tibio-basitarsal joint flexes. The auricle swings up against the underside of the tibial apex, and the trapped pollen is squeezed outward and upward, past the rastellum, onto the lower end of the bare corbicular floor.6566

Grow. The next press pushes a new layer in from below, lifting the earlier pollen up the plate. The oldest pollen ends up at the top of the load, near the femur, and the fringe hairs on both rims are progressively buried in the mass. The midlegs pat the sides as it grows.69

The rastellum, auricle and press were described in the honey bee in detail. Bumblebees carry the same rake, the same flange and the same flexing joint, and Sladen watched them load from the bottom up in the same way.64 Where the two genera differ, in the tibial spurs and in the basket hairs, the drawings follow Bombus.

Two separate questions hide in the word basket. What holds the pollen mass together, and what attaches it to the leg. Nothing closes over the load; in cross-section the loaded tibia is a shallow lens with the load standing as a dome on its outer face, well proud of the leg. So the answer to neither question is containment.

Held together. The mass coheres because it is wet. The sugar solution from the crop forms liquid bridges between spiny, pollenkitt-coated grains, and a moist granular mass of that kind holds its shape. In the honey bee the finished pellet has been measured as a viscoelastic solid with a long relaxation time, which is why it keeps its form through a foraging trip.78

The balance of forces has not been measured for bumblebee loads. Liquid bridging is the likely basis of cohesion here, not a demonstrated one.

Held on. The same honey bee study pulled pellets off the leg and found the corbicular fringe hairs embedded in the pellet, and inferred that those hairs are the principal source of attachment force.78 That is a different picture from a sticky dome adhering to a smooth floor with the hairs steadying its edges: the hairs run into the mass and hold it. The sixth figure is drawn that way. The bumblebee corbicula is rimmed by the same kind of long curved hairs, with the entrance hairs at its base, and the measurement has been made only in Apis.

Each arrow in the seventh figure is one transfer between body parts, and the labelled step is the action that makes it. The mouthparts and crop feed fluid into the stream at the forelegs. Pollen collected directly from the abdomen or the legs need not pass through the whole head, foreleg and midleg sequence; it joins at the hind basitarsus. The midlegs both pass pollen forward and, later, shape the load.6569

Everything above is about food. The packed loads are pollen the bee is carrying home to feed larvae, and pollen that has been wetted, pressed and packed is no longer available to any flower. Pollination is a different outcome: it depends on pollen that stays loose on the body and is carried to the stigma of the next flower.71

The two outcomes coexist on one bee because grooming is not complete. Koch, Lunau and Wester dusted anthers and stigmas with fluorescent dye and let honey bees and bumblebees forage; the bees came away with dye on the same body patches every time, places the legs cannot reach, and those same patches were the ones that touched stigmas.77 The plumose pile therefore does two jobs at once. Most of what it catches is combed off and packed. What it holds in the ungroomed patches is what the goldenrod gets in return.