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Article history:
Received 30 May 2011
Accepted 27 June 2011
We have re-investigated the organization of ocelli in honeybee workers and drones. Ocellar lenses are
divided into a dorsal and a ventral part by a cusp-shaped indentation. The retina is also divided, with
a ventral retina looking skywards and a dorsal retina looking at the horizon. The focal plane of lenses lies
behind the retina in lateral ocelli, but within the dorsal retina in the median ocellus of both workers and
drones. Ventral retinula cells are ca. 25 mm long with dense screening pigments. Dorsal retinula cells are
ca. 60 mm long with sparse pigmentation mainly restricted to their proximal parts. Pairs of retinula cells
form at, non-twisting rhabdom sheets with elongated, straight, rectangular cross-sections, on average
8.7 mm long and 1 mm wide. Honeybee ocellar rhabdoms have shorter and straighter cross-sections than
those recently described in the night-active bee Megalopta genalis. Across the retina, rhabdoms form
a fan-shaped pattern of orientations. In each ocellus, ventral and dorsal retinula cell axons project into
two separate neuropils, converging on few large neurons in the dorsal, and on many small neurons in the
ventral neuropil. The divided nature of the ocelli, together with the particular construction and
arrangement of rhabdoms, suggest that ocelli are not only involved in attitude control, but might also
provide skylight polarization compass information.
2011 Elsevier Ltd. All rights reserved.
Keywords:
Honeybees
Workers
Drones
Ocelli
Rhabdom organization
Polarization sensitivity
1. Introduction
In addition to the compound eyes, many insects possess three
single lens eyes, called ocelli (e.g. Wilson, 1975; Goodman, 1981;
Warrant et al., 2006; Berry et al., 2007a; reviewed by Mizunami,
1994). An ocellus typically consist of a lens, a vitreous body, an
iris, a corneageneous cell layer, a retina (including pigment cells)
and a neuropil in which photoreceptor axons make contact with
interneurons (Goodman, 1981).
Ocelli typically possess large elds of view and are usually
found to be heavily under-focused, although in some species the
optical focal plane lies in or near the retina (e.g. ies: Schuppe
and Hengstenberg, 1993; dragonies: Stange et al., 2002; Berry
et al., 2007a,c; locusts: Berry et al., 2007b; bees and wasps:
Warrant et al., 2006). Photoreceptors typically have spectral
sensitivities peaking in the UV and green (e.g. Wilson, 1975;
Geiser and Labhart, 1982; van Kleef et al., 2005; Berry et al.,
510
511
2.1. Histology
2.5. Optics
The back focal distances and the focal lengths of ocellar lenses
were measured using a modication of Homanns (1924) hanging
drop method (see Warrant et al., 2006 for a more detailed
description of the method). A small piece of cuticle containing
either a lateral or a median ocellus was carefully dissected from
the head capsule of a freshly killed bee and placed in 0.9% sodium
chloride solution. All tissue was removed from the inner side of
the ocellar lens with a ne brush. The lens was then placed on
a droplet of physiological saline on a cover slip, in such a way that
its external surface remained in air. To prevent evaporation, we
constructed a chamber by mounting an O-ring on a microscope
slide. We then covered the upper side of the ring with a thin layer
Fig. 1. The ocelli of worker honeybees. (a) Frontal view. The median ocellus (arrow) is placed dorsally between the two compound eyes and looks upwards and forwards. The two
lateral ocelli are not visible, being completely covered by dense, long hairs. Scale bar 1 mm. (b) Side view. The restricted visual eld of the right lateral ocellus (arrow) is determined
by a special hair-free zone which gives the lateral ocelli clear view to the side and upwards. d: dorsal; p: posterior; Scale bar 1 mm. (c) Scanning electron micrograph frontal view of
worker bee ocelli with all hairs on the head capsule and the compound eyes having been removed. The normally hair-free zones at the ventral side of the ocelli can be recognized as
distinct patterns of smooth (at) cuticle, due to the lack of hair sockets (arrows). Scale bar 1 mm. (d) Dorsal view. The two lateral ocelli are clearly visible. Note the hair-free zones
providing unobstructed lateral and dorsal elds of view. Scale bar 1 mm. (e) Frontal view of a head replica. Hair-free zones (hfz) are clearly distinguishable from those regions of the
head that are normally covered by hairs (note hair sockets). ce: compound eye; hfz: hair-free zones mo: median ocellus; lo: lateral ocellus. Scale bar 300 mm.
512
of Vaseline. The cover slip was placed upside-down (with the lens
directed downwards) onto the O-ring. The back focal plane of the
lens was viewed through the cover slip and the saline with the
25 objective of a Zeiss microscope with the condenser removed.
A pattern of black-and-white stripes, made from translucent paper
and black tape pieces, was placed over the lamp in the microscope
foot at a distance s from the ocellar lens (s 113 mm). The spatial
wavelength lo of the stripe pattern was 8 mm. We then determined the position of best focus of the image of the stripe pattern
behind the ocellar lens. The spatial wavelength li of the image (in
mm), the spatial wavelength of the object lo and the object
distance s then allowed us to calculate the focal length f of the
ocellar lens:
f sli =lo
The nodal point N is situated at a distance of one focal length f in
front of the image and its position within the ocellar lens was
determined by measuring the back focal distance of the lens, that is,
the distance from the image to the back of the lens (as determined
by the calibrated focussing knob of the microscope) multiplied by
1.34 to correct for the refractive index of the saline droplet. The
distance of the nodal point from the proximal edge of the ocellar
lens is then simply the back focal distance subtracted from the focal
length.
2.6. Visual elds
The visual elds of ocelli were estimated by mounting worker
and drone bee heads with an insect pin on a goniometer. We
dened the vertical axis of the head as the line from the centre of
the median ocellus through the proboscis and the horizontal axis as
the line from the occipital opening to the centre of the basal scape
of the two antennae. Note, however, that the head posture of bees is
likely to differ depending on their ight speed and state of locomotion. We used the visibility of ocelli when heads were turned
through dened angles under a dissection microscope as a rough
measure of the maximal extent of visual elds.
3. Results
3.1. External morphology and visual elds
In the worker bee the three ocelli form an equilateral triangle
positioned on the apex of the head (Fig. 1c and d). In drones, the
three ocelli are slightly larger, sit closer together and are positioned
more frontally, squeezed in between the giant compound eyes
(Fig. 2). Ocellar lenses in both worker and drone bees have a slightly
ellipsoid shape (Figs. 1e and 2c), with major axes in the lateral ocelli
of the worker bee in the anterior-posterior direction and in the
ventral dorsal direction in the drone. The median ocellus is nearly
circularly symmetric in both sexes (Table 1).
The dense cover of hair on the worker and drone head make the
ocelli hard to recognize (Figs. 1a, b and 2a), although the head
cuticle just lateral of the lateral ocelli and just ventral of the median
ocellus is smooth and free of hairs (Figs. 1 and 2). Dense hair tufts
overlying the median ocellus on the worker bee head separate the
visual elds of all three ocelli in the horizontal direction and shade
the median ocellus from above (Fig. 1a and d). In the drone the
three ocelli are located at the very front of the head and are
arranged closely together (Fig. 2). They are also surrounded by
densely packed hairs that, however, leave an unobstructed view in
the frontal-ventral direction. In both worker and drone bees,
a special patch of dense, long hairs between the three ocelli limits
the visual eld in the dorsal direction.
The hairs around the ocelli act as a set of visors and shield the
median ocellus against direct sunlight from above. In the case of the
lateral ocelli, the surrounding hairs allow light to enter only from
the side and from above. The visibility of the ocellar lenses thus
allows us to roughly estimate their visual elds. The median ocellus
of the worker bee is invisible when the head is viewed directly from
the front, whereas it is fully visible when viewed from 20 above
the horizontal. At 30 above the horizontal the ocellus is covered
dorsally by hairs and when viewed at 40 it is no longer visible from
above. In elevation, the visual eld is centred at 25 above the
horizontal plane of the head and has a horizontal extent of
approximately 40 . The lateral ocelli only become visible at elevations larger than 50 and in azimuth they are fully visible 70
away from the midline. The centres of their visual elds therefore
lie approximately 70 to either side of the midline at an elevation
of 55 .
We investigated bees of different ages (16 d, 18 d, 23 d, 25 d) to
check whether the density of the hairs around the ocelli may be
subject to wear and tear, and thereby modify the visual eld.
However, we did not nd noticeable differences in hair cover in the
different ages of worker bees.
The ocelli of the drone look to the front and ventrally. Viewed
from straight ahead, a dense patch of hair completely obscures the
drone median ocellus but it is fully visible at an elevation of 15
below the horizon. In elevation, the visual eld of the drone median
ocellus is centred about 10 below the horizon with a horizontal
visual eld of approximately 25 either side of the midline. The
lateral ocelli become visible at about 10 azimuth either side of the
midline and their full extent is seen at 50 on either side of the
midline. The centres of their visual elds thus approximately view
the horizon over 45 on either side of the midline. Note, however,
that workers and possibly also drones hold their heads pitched
upwards in ight (e.g. Wehner, 1972; van Praagh et al., 1980).
3.2. Corneal lenses
The ocellar lenses are thickened areas of transparent cuticle
distal to the ocellar retinae and neuropils (Fig. 3). Frontal sections
through the lateral ocelli show a biconvex, thick lens with a cuspshaped (bipartite) outer surface and an asymmetrical inner
surface (Fig. 3aec). The shape of the corneal lens of the median
ocellus has the same cusp-shaped outer surface. Median and lateral
ocellar corneal replicas and SEM micrographs show a distinct
surface pattern in both sexes: a rough, uneven region with an
ellipsoid to roundish shape, covering two thirds of the lens surface
(Figs. 1e and 2c).
3.3. Optical properties of ocellar lenses
Focal length measurements were made from the lateral and
medial ocelli of two drones and three workers. Images formed
behind the corneal lenses were typically blurry and, compared with
the original striped object, of considerably reduced contrast. In all
cases, the measured focal lengths based on these images indicate
that lateral ocelli in both castes are heavily under-focused, that is,
the focal plane of the corneal lens lies behind the retina (Fig. 4, left
panels). The situation is different in the median ocelli where the
focal plane lies within the dorsal, but not the ventral retina (Fig. 4,
right panels). Due to the nature of the hanging drop method (in
which lens position on the drop is decided by gravity), the
measurements described below were unable to distinguish the
optical properties of different parts of the bipartite ocellar lens.
However, such differences may exist, as suggested by the division of
the ocellar retina into distinct dorsal and ventral regions (see
below).
513
Fig. 2. The ocelli of drone honeybees. (a) Frontal view. The three ocelli are arranged in a small triangle in a hair-free zone at the front of the head. The median ocellus (mo) is slightly
larger than the two lateral ocelli (lo), which are laterally constricted by the huge compound eyes (ce). The eld of view dorsally and ventrally is obscured by dense tuffs of hair. Scale
bar 1 mm. (b) Scanning electron micrograph of the dorsal view of the shaved drone head. The three ocelli sit on a raised part of the cuticle. The bulging compound eyes restrict the
ocellar eld of views in lateral directions. p: posterior. Scale bar 1 mm. (c) Frontal view of a drone replica. The ocelli of drones are slightly larger than those of the worker bee, sit
closer together on the front of the head, and are packed tightly between the giant compound eyes. Ocellar lenses have a rough surface and are surrounded by cuticle studded with
hair sockets (hs). d: dorsal. Scale bar 500 mm.
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Table 1
Anatomical dimensions of lateral and median ocelli in honeybee workers and
drones.
Worker
Drone
3.76 0.07
293 6
315 4
264 5
295 21
4.39 0.13
305 3
396 4
364 6
372 3
Notes: for all measurements n 5; head size was measured as the frontal diameter
of the head, between the lateral edges of the compound eyes.
Fig. 3. Histology of honeybee ocelli. (a) Semi-thin frontal section of a worker honeybee brain, showing the two lateral ocelli above the four calyces of the mushroom bodies. Note the
cusp in the outer surface of ocellar lenses (arrows). Section plane 42 mm from the front, stained with toluidine blue. ca: calyx of the median mushroom body; lo: lateral ocellus; mon:
neuropile of the median ocellus. Scale bar 100 mm. (b) Frontal section of a worker honeybee lateral ocellus. d: dorsal; dr: dorsal retina; i: iris; l: lens; v: ventral; vr: ventral retina.
Scale bar 100 mm. (c) Vertical section through the drone lateral ocellus. Note the cusp-shaped surface of the lens (arrow). Retinula cells in the dorsal retina (dr) are much longer than
in the ventral retina (vr) and their pigmentation is less dense compared with the ventral retina. vb: vitreous body; lcl: lens cell layer. Scale bar 50 mm. (d) Frontal section of a worker
lateral ocellus. kc: Kenyon cells of the mushroom body; rca: receptor cell axons; rcb: retinula cell bodies; sp: screening pigment. Scale bar 25 mm.
515
Fig. 4. Schematic diagram of ocellar optics in honeybee drones and workers as determined by the hanging drop technique (see Materials and methods and Results for details). The
focal plane is indicated by the dashed line relative to the nodal point (N). The lens is shown in orange, the vitreous body in yellow, the dorsal retina in dark green and the ventral
retina in light green. Note that in both drones and workers, the focal plane in lateral ocelli lies proximal to both the ventral and the dorsal retina, while it lies within the dorsal retina
in the median ocelli (For interpretation of the references to colour in this gure legend, the reader is referred to the web version of this article.).
516
Fig. 5. The ocellar retina. (a) Cross-section of a retina of a worker lateral ocellus. Each
elongated rhabdom (arrows) is formed by two rhabdomeres of adjacent retinula cells
(circle). The rhabdoms are oriented in a fan-shaped pattern across the retina. Scale bar
20 mm. (b) How rhabdoms are arranged across the worker retina and their potential
polarization sensitivity. Red dots mark the ve points along each rhabdom that were
determined according to inset of Fig. 6a. Blue lines are perpendicular to the long axis of
rhabdom cross-sections and indicate the direction of maximal potential polarization
sensitivity of each rhabdom (for details see text) (For interpretation of the references to
colour in this gure legend, the reader is referred to the web version of this article.).
517
Fig. 6. The properties of ocellar rhabdoms. For each of 95 rhabdoms in the worker ocellar retina, the straightness of the cross-section was determined by measuring the deviation of
the orientation of four segments along the rhabdom from the line connecting the two end points as shown in the upper inset in (a). (a) Frequency distribution of the mean absolute
segment deviation per rhabdom. The lower inset shows expected means for different amounts of curvature of a hypothetical rhabdom. (b) Frequency distribution of all signed
segment deviations from the orientation of the line connecting the two end points of a rhabdom. (c) Overall rhabdom orientations relative to horizontal (0 ) across the retina. (d)
Frequency distribution of rhabdom length.
Fig. 7. Tangential section of a worker lateral ocellus. Each part of the bipartite retina
gives rise to a separate axon bundle (dorsal and ventral plexus). kc: Kenyon cells of the
mushroom body; a: anterior. Otherwise conventions as before. Scale bar 25 mm.
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Fig. 8. A comparison of rhabdom properties between honeybees and the night-active bee Megalopta (histological material of Megalopta was kindly provided by Richard Berry and
Eric Warrant (see Berry et al., 2011)). (a) A comparison of the straightness of rhabdom cross-sections as measured by the mean absolute deviation of rhabdom segments per
rhabdom from the line connecting the two end points of rhabdom cross-sections. Inset shows the distribution of segment deviations (mean of all absolute segment deviations:
honeybee, 9.3 7.6 ; Megalopta, 19.7 15.1 ). Note that honeybee rhabdom cross-sections are much straighter than those in Megalopta. Rhabdoms in Megalopta were divided into 8
segments of equal length. (b) Frequency distributions of rhabdom length in honeybees and Megalopta. Honeybee rhabdoms are much shorter (8.7 2.4 mm, n 95) than those of
Megalopta (14.3 3.5 mm, n 84). (c) A horizontal cross-section through the retina of the median ocellus of Megalopta (semi-thin cross-section kindly provided by Richard Berry;
from Berry et al., 2011). Rhabdoms are emphasized by black lines. A few short and straight rhabdoms are labelled white (see text for explanation). Scale bar 20 mm. (d) A horizontal
cross-section through the retina of the median ocellus of a honeybee worker. Conventions as in (c).
519
Acknowledgements
We thank Paul Helliwell and Ryszard Maleszka for the supply
of bees, the ANUs Centre for Advanced Microscopy for the use of
their facilities and Waltraud Pix for her help with analysing
rhabdom shapes and dimensions. We thank two reviewers for
their constructive comments. This work received nancial support
in the form of Visiting Fellowships from the Centre for Visual
Sciences to WR and from the ARC Centre of Excellence in Vision
Science to EW and WR. We acknowledge additional support from
the Private University of Liechtenstein, the Swedish Research
Council, the US Air Force of Scientic Research (AFOSR: Grant No.
FA8655-07-C-4011) and the ARC Centre of Excellence in Vision
Science.
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