Transcriber's Note
Text emphasis for italics is represented by _Text_.
* * * * *
U. S. DEPARTMENT OF AGRICULTURE,
BUREAU OF ENTOMOLOGY--BULLETIN No. 121.
L. O. HOWARD. Entomologist and Chief of Bureau.
THE BEHAVIOR OF THE HONEY BEE
IN POLLEN COLLECTING.
BY
D. B. CASTEEL, Ph. D.,
_Collaborator and Adjunct Professor of Zoology,_
_University of Texas._
Issued December 31, 1912.
[Illustration]
WASHINGTON:
GOVERNMENT PRINTING OFFICE.
1912.
_BUREAU OF ENTOMOLOGY._
L. O. Howard, _Entomologist and Chief of Bureau_.
C. L. Marlatt, _Entomologist and Acting Chief in Absence of Chief_.
R. S. Clifton, _Executive Assistant_.
W. F. Tastet, _Chief Clerk_.
F. H. Chittenden, _in charge of truck crop and stored product insect
investigations_.
A. D. Hopkins, _in charge of forest insect investigations_.
W. D. Hunter, _in charge of southern field crop insect investigations_.
F. M. Webster, _in charge of cereal and forage insect investigations_.
A. L. Quaintance, _in charge of deciduous fruit insect investigations_.
E. F. Phillips, _in charge of bee culture_.
D. M. Rogers, _in charge of preventing spread of moths, field work_.
Rolla P. Currie, _in charge of editorial work_.
Mabel Colcord, _in charge of library_.
Investigations in Bee Culture.
E. F. Phillips, _in charge_.
G. F. White, J. A. Nelson, _experts_.
G. S. Demuth, A. H. McCray, N. E. McIndoo, _apicultural assistants_.
Pearle H. Garrison, preparator.
D. B. Casteel, collaborator.
LETTER OF TRANSMITTAL.
U. S. Department of Agriculture,
Bureau of Entomology,
_Washington, D. C, September 23, 1912_.
Sir: I have the honor to transmit herewith a manuscript entitled "The
Behavior of the Honey Bee in Pollen Collecting," by Dr. Dana B.
Casteel, of this bureau. The value of the honey bee in cross
pollinating the flowers of fruit trees makes it desirable that exact
information be available concerning the actions of the bee when
gathering and manipulating the pollen. The results recorded in this
manuscript are also of value as studies in the behavior of the bee and
will prove interesting and valuable to the bee keeper. The work here
recorded was done by Dr. Casteel during the summers of 1911 and 1912
at the apiary of this bureau.
I recommend that this manuscript be published as Bulletin No. 121
of the Bureau of Entomology.
Respectfully,
L. O. Howard,
_Entomologist and Chief of Bureau_.
Hon. James Wilson,
_Secretary of Agriculture_.
CONTENTS.
Page.
Introduction 7
The structures concerned in the manipulation of pollen 7
The pollen supply 10
General statement of the pollen-collecting process 11
Action of the forelegs and mouthparts 13
Action of the middle legs 14
Action of the hind legs 16
Additional details of the basket-loading process 18
Pollen moistening 22
Storing pollen in the hive 29
Summary 31
Bibliography 33
Index 35
ILLUSTRATIONS.
TEXT FIGURES.
Page.
Fig. 1. Left foreleg of a worker bee 8
2. Left middle leg of a worker bee 9
3. Outer surface of the left hind leg of a worker bee 10
4. Inner surface of the left hind leg of a worker bee 11
5. A flying bee, showing the manner in which the forelegs
and middle legs manipulate pollen 14
6. A bee upon the wing, showing the position of the middle
legs when they touch and pat down the pollen masses 15
7. A bee upon the wing, showing the manner in which the
hind legs are held during the basket-loading process 17
8. The left hind legs of worker bees, showing the manner
in which pollen enters the basket 19
9. Inner surface of the right hind leg of a worker bee
which bears a complete load of pollen 22
THE BEHAVIOR OF THE HONEY BEE IN POLLEN COLLECTING.
INTRODUCTION.
While working upon the problem of wax-scale manipulation during the
summer of 1911 the writer became convinced that the so-called wax
shears or pinchers of the worker honey bee have nothing whatever to do
with the extraction of the wax scales from their pockets, but rather
that they are organs used in loading the pollen from the pollen combs
of the hind legs into the corbiculæ or pollen baskets (Cast eel,
1912). Further observations made at that time disclosed the exact
method by which the hind legs are instrumental in the pollen-loading
process and also the way in which the middle legs aid the hind legs in
patting down the pollen masses. During the summer of 1912 additional
information was secured, more particularly that relating to the manner
in which pollen is collected upon the body and legs of the bee, how it
is transferred to the hind legs, how it is moistened, and finally the
method by which it is stored in the hive for future use. In the
present paper a complete account will be given of the history of the
pollen from the time it leaves the flower until it rests within the
cells of the hive. The points of more particular interest in the
description of pollen manipulation refer to (1) the movements
concerned in gathering the pollen from the flowers upon the body and
legs, (2) the method by which the baskets of the hind legs receive the
loads which they carry to the hive, and (3) the manner in which the
bee moistens pollen and renders it sufficiently cohesive for packing
and transportation.
THE STRUCTURES CONCERNED IN THE MANIPULATION OF POLLEN.
The hairs which cover the body and appendages of the bee are of the
utmost importance in the process of pollen gathering. For the purposes
of this account these hairs may be classified roughly 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 antennæ 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. Although, as above noted,
some unbranched hairs are located upon the body of the bee, they occur
in greatest numbers upon the more distal segments of the appendages.
They are quite diverse in form, some being extremely long and slender,
such as those which curve over the pollen baskets, others being stout
and stiff, as those which form the collecting brushes and the pecten
spines.
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 maxillæ 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,
unbranched hairs set closely together. These brushes are located upon
the first or most proximal tarsal segment of the legs, known
technically as the palmæ of the forelegs and as the plantæ of the
middle and hind pair. The brush of the foreleg is elongated and of
slight width (fig. 1), that of the middle leg broad and flat (fig. 2),
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 tibiæ 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.
[Illustration: Fig. 1.--Left foreleg of a worker bee. (Original.)]
The tibia and the planta of the hind leg of the worker bee are greatly
flattened. (See figs. 3, 4.) 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 to 21 in number, which form the pecten or comb of the tibia. The
lateral edge of this area forms the lower boundary of the corbicula r
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, are found 7 or 8 minute spines, 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 the wax scales (Casteel, 1912). 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 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.
[Illustration: Fig. 2.--Left middle leg of a worker bee. (Original.)]
THE POLLEN SUPPLY.
When bees collect pollen from flowers they may be engaged in this
occupation alone or may combine it with nectar gathering. From some
flowers the bees take only nectar, from others only pollen; a third
class of flowers furnishes an available supply of both of these
substances. But even where both pollen and nectar are obtainable a bee
may gather nectar and disregard the pollen. This is well illustrated
by the case of white clover. If bees are watched while working upon
clover flowers, the observer will soon perceive some which bear pollen
masses upon their hind legs, while others will continue to visit
flower after flower, dipping into the blossoms and securing a
plentiful supply of nectar, yet entirely neglecting the pollen.
[Illustration: Fig. 3.--Outer surface of the left hind leg of a worker
bee. (Original.)]
The supply of pollen which is available for the bees varies greatly
among different flowers. Some furnish an abundant amount and present
it to the bee in such a way that little difficulty is experienced in
quickly securing an ample load, while others furnish but little. When
flowers are small and when the bee approaches them from above, little,
if any, pollen is scattered over the bee's body, all that it acquires
being first collected upon the mouth and neighboring parts, of a Very
different conditions are met with when bees visit such plants as corn
and ragweed. The flowers of these plants are pendent and possess an
abundant supply of pollen, which falls in showers over the bodies of
the bees as they crawl beneath the blossoms. The supply of pollen
which lodges upon the body of the bee will thus differ considerably in
amount, depending upon the type of flower from which the bee is
collecting, and the same is true regarding the location upon the body
of a bee of pollen grains which are available for storage in the
baskets. Moreover, the movements concerned in the collection of the
pollen from the various body parts of the bee upon which it lodges
will differ somewhat in the two cases, since a widely scattered supply
requires for its collection additional movements, somewhat similar in
nature to those which the bee employs in cleaning the hairs which
cover its body.
[Illustration: Fig. 4.--Inner surface of the left hind leg of a worker
bee. (Original.)]
GENERAL STATEMENT OF THE POLLEN-COLLECTING PROCESS.
A very complete knowledge of the pollen-gathering behavior of the
worker honey bee may be obtained by a study of the actions of bees
which are working upon a plant which yields pollen in abundance. Sweet
corn is an ideal plant for this purpose, and it will be used as a
basis for the description which follows.
In attempting to outline the method by which pollen is manipulated the
writer wishes it to be understood that he is recounting that which he
has seen and that the description is not necessarily complete,
although he is of the opinion that it is very nearly so. The movements
of the legs and of the mouthparts are so rapid and so many members
are in action at once that it is impossible for the eye to follow all
at the same time. However, long-continued observation, assisted by the
study of instantaneous photographs, gives confidence that the
statements recorded are accurate, although some movements may have
escaped notice.
To obtain pollen from corn the bee must find a tassel in the right
stage of ripeness, with flowers open and stamens hanging from them.
The bee alights upon a spike and crawls along it, clinging to the
pendent anthers. It crawls over the anthers, going from one flower to
another along the spike, being all the while busily engaged in the
task of obtaining pollen. This reaches its body in several ways.
As the bee moves over the anthers it uses its mandibles and tongue,
biting the anthers and licking them and securing a considerable amount
of pollen upon these parts. This pollen becomes moist and sticky,
since it is mingled with fluid from the mouth. A considerable amount
of pollen is dislodged from the anthers as the bee moves over them.
All of the legs receive a supply of this free pollen and much adheres
to the hairs which cover the body, more particularly to those upon the
ventral surface. This free pollen is dry and powdery and is very
different in appearance from the moist pollen masses with which the
bee returns to the hive. Before the return journey this pollen must be
transferred to the baskets and securely packed in them.
After the bee has traversed a few flowers along the spike and has
become well supplied with free pollen it begins to collect it from its
body, head, and forward appendages and to transfer it to the posterior
pair of legs. This may be accomplished while the bee is resting upon
the flower or while it is hovering in the air before seeking
additional pollen. It is probably more thoroughly and rapidly
accomplished while the bee is in the air, since all of the legs are
then free to function in the gathering process.
If the collecting bee is seized with forceps and examined after it has
crawled over the stamens of a few flowers of the corn, its legs and
the ventral surface of its body are found to be thickly powdered over
with pollen. If the bee hovers in the air for a few moments and is
then examined very little pollen is found upon the body or upon the
legs, except the masses within the pollen baskets. While in the air it
has accomplished the work of collecting some of the scattered grains
and of storing them in the baskets, while others have been brushed
from the body.
In attempting to describe the movements by which this result is
accomplished it will be best first to sketch briefly the roles of the
three pairs of legs. They are as follows:
(_a_) The first pair of legs remove scattered pollen from the head and
the region of the neck, and the pollen that has been moistened by
fluid substances from the mouth.
(_b_) The second pair of legs remove scattered pollen from the thorax,
more particularly from the ventral region, and they received the
pollen that has been collected by the first pair of legs.
(_c_) The third pair of legs collect a little of the scattered pollen
from the abdomen and they receive pollen that has been collected by
the second pair. Nearly all of this pollen is collected by the pollen
combs of the hind legs, and is transferred from the combs to the
pollen baskets or corbiculæ in a manner to be described later.
It will thus be seen that the manipulation of pollen is a successive
process, and that most of the pollen at least passes backward from the
point where it happens to touch the bee until it finally reaches the
corbiculæ or is accidentally dislodged and falls from the rapidly
moving limbs.
ACTION OF THE FORELEGS AND MOUTHPARTS.
Although the pollen of some plants appears to be somewhat sticky, it
may be stated that as a general rule pollen can not be successfully
manipulated and packed in the baskets without the addition of some
fluid substance, preferably a fluid which will cause the grains to
cohere. This fluid, the nature of which will be considered later,
comes from the mouth of the bee, and is added to the pollen which is
collected by the mouthparts and to that which is brought into contact
with the protruding tongue and maxillæ, and, as will appear, this
fluid also becomes more generally distributed upon the legs and upon
the ventral surface of the collecting bee.
When a bee is collecting from the flowers of corn the mandibles are
actively engaged in seizing, biting, and scraping the anthers as the
bee crawls over the pendent stamens. Usually, but not always, the
tongue is protruded and wipes over the stamens, collecting pollen and
moistening the grains thus secured. Some of the pollen may possibly be
taken into the mouth. All of the pollen which comes in contact with
the mouthparts is thoroughly moistened, receiving more fluid than is
necessary for rendering the grains cohesive. This exceedingly wet
pollen is removed from the mouthparts by the forelegs (fig. 5), and
probably the middle legs also secure a little of it directly, since
they sometimes brush over the lower surface of the face and the mouth.
In addition to removing the very moist pollen from the mouth the
forelegs also execute cleansing movements over the sides of the head
and neck and the anterior region of the thorax, thereby collecting
upon their brushes a considerable amount of pollen which has fallen
directly upon these regions, and this is added to the pollen moistened
from the mouth, thereby becoming moist by contact. The brushes of the
forelegs also come in contact with the anterior breast region, and the
hairs which cover this area become moist with the sticky exudation
which the forelegs have acquired in the process of wiping pollen from
the tongue, maxillæ, and mandibles.
ACTION OF THE MIDDLE LEGS.
The middle legs are used to collect the pollen gathered by the
forelegs and mouthparts, to remove free pollen from the thoracic
region, and to transport their load of pollen to the hind legs,
placing most of it upon the pollen combs of these legs, although a
slight amount is directly added to the pollen masses in the corbiculæ.
Most of the pollen of the middle legs is gathered upon the conspicuous
brushes of the first tarsal segments or plantæ of these legs.
[Illustration: Fig. 5.--A flying bee, showing the manner in which the
forelegs and middle legs manipulate pollen. The forelegs are removing
wet pollen from the mouthparts and face. The middle leg of the right
side is transferring the pollen upon its brush to the pollen combs of
the left hind planta. A small amount of pollen has already been placed
in the baskets. (Original.)]
In taking pollen from a foreleg the middle leg of the same side is
extended in a forward direction and is either grasped by the flexed
foreleg or rubbed over the foreleg as it is bent downward and
backward. In the former movement the foreleg flexes sharply upon
itself until the tarsal brush and coxa nearly meet. The collecting
brush of the middle leg is now thrust in between the tarsus and coxa
of the foreleg and wipes off some of the pollen from the foreleg
brush. The middle leg brush is then raised and combs down over the
flexed foreleg, thus removing additional pollen from the outer surface
of this leg. The middle leg also at times reaches far forward,
stroking down over the foreleg before it is entirely flexed and
apparently combing over with its tarsal brush the face and mouthparts
themselves. When the middle leg reaches forward to execute any of the
above movements the direction of the stroke is outward, forward, and
then back toward the body, the action ending with the brush of the leg
in contact with the long hairs of the breast and with those which
spring from the proximal segments of the forelegs (coxa, trochanter,
femur). As a result of the oft-repeated contact of the brushes of the
middle and forelegs with the breast, the long, branched hairs which
cover this region become quite moist and sticky, since the brushes of
these two pair of legs are wet and the pollen which they bear
possesses a superabundance of the moistening fluid. Any dry pollen
which passes over this region and touches these hairs receives
moisture by contact with them. This is particularly true of the free
dry pollen which the middle pair of legs collect by combing over the
sides of the thorax.
[Illustration: Fig. 6.--A bee upon the wing, showing the position of
the middle legs when they touch and pat down the pollen masses. A very
slight amount of pollen reaches the corbiculæ through this movement.
(Original.)]
The pollen upon the middle legs is transferred to the hind legs in at
least two ways. By far the larger amount is deposited upon the pollen
combs which lie on the inner surfaces of the plantæ of the hind legs.
To accomplish this a middle leg is placed between the plantæ of the
two hind legs, which are brought together so as to grasp the brush of
the middle leg, pressing it closely between them, but allowing it to
be drawn toward the body between the pollen combs of the two hind
legs. (See fig. 5.) This action results in the transference of the
pollen from the middle-leg brush to the pollen combs of the hind leg
of the opposite side, since the combs of that leg scrape over the
pollen-laden brush of the middle leg. This action may take place while
the bee is on the wing or before it leaves the flower.
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.
[Illustration: Fig. 7.--A bee upon the wing, showing the manner in
which the hind legs are held during the basket-loading process. Pollen
is being scraped by the pecten spines of the right leg from the pollen
combs of the left hind planta. (Original.)]
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.
[Illustration: Fig. 8.--Camera drawings of the left hind legs of
worker bees to show the manner in which pollen enters the basket. _a_,
Shows a leg taken from a bee which is just beginning to collect. It
had crawled over a few flowers and had flown in the air about five
seconds at the time of capture. The pollen mass lies at the entrance
of the basket, covering over the fine hairs which lie along this
margin and the seven or eight short stiff spines which spring from the
floor of the corbicula immediately above its lower edge. As yet the
pollen has not come in contact with the one long hair which rises from
the floor and arches over the entrance. The planta is extended, thus
lowering the auricle; _b_, represents a slightly later stage, showing
the increase of pollen. The planta is flexed, raising the auricle. The
hairs which extend outward and upward from the lateral edge of the
auricle press upon the lower and outer surface of the small pollen
mass, retaining it and guiding it upward into the basket; _c_, _d_,
represent slightly later stages in the successive processes by which
additional pollen enters the basket. (Original.)]
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.
[Illustration: Fig. 9.--Inner surface of the right hind leg of a
worker bee which bears a complete load of pollen, _a_, Scratches in
the pollen mass caused by the pressure of the long projecting hairs of
the basket upon the pollen mass as it has been pushed up from below;
_b_, groove in the pollen mass made by the strokes of the auricle as
the mass projects outward and backward from the basket. (Original.)]
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.
The writer is not prepared to deny the possibility that the surface of
the chitin of the hind legs of worker bees may be moistened by the
secretion of glands which lie beneath it, but he is convinced that any
fluid thus secreted bears little or no relation to the cohesion of the
pollen grains within the baskets. Sections and dissected preparations
of the hind legs of worker bees show certain large cells which lie
within the cavity of the leg and which may function as secreting gland
cells; but similar structures occur in even greater numbers within the
hind legs of the drone and they are found within the hind legs of the
queen.
As has been noted, the extreme moisture of the plantar combs and of
the tibio-tarsal articulation of the hind leg is readily understood
when one recalls the manner in which moist pollen is compressed
between the auricle and the tibial surface above it.
From the account already given it is evident that, in the opinion of
the writer, the mouth is the source from which the pollen-moistening
fluid is obtained. It is extremely difficult to determine with
absolute accuracy the essential steps involved in the process of
adding moisture to the pollen. In an endeavor to solve this problem
the observer must of necessity consider a number of factors, among
which may be noted (1) the location upon the body of the collecting
bee of "moist" and of comparatively "dry" pollen, (2) the movements
concerned in the pollen-gathering and pollen-transferring processes,
(3) the relative moisture of those parts which handle pollen, (4) the
chemical differences between the natural pollen of the flower and that
of the corbiculæ and of the cells of the hive, and (5) the observer
must endeavor to distinguish between essential phenomena and those
which are merely incidental or accidental.