Twilight orientation to polarised light in the crepuscular dung beetle Scarabaeus zambesianus
1 Department of Cell and Organism Biology, University of Lund,
Helgonavägen 3, S-223 62 Lund, Sweden
2 Department of Zoology and Entomology, University of Pretoria, South
Africa
* Author for correspondence (e-mail: marie.dacke{at}cob.lu.se)
Accepted 12 February 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: dung beetle, Scarabaeus zambesianus, orientation, ommatidia, receptor, rhabdom, polarisation pattern, skylight.
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Also present in the sky, but not visible to humans, is the pattern of
polarised skylight centred on the sun. During the course of the day, this
pattern of polarised light changes its appearance with the apparent movement
of the sun. During twilight, the pattern is most simple, with the light of the
whole sky polarised in one direction. The zenith of the sky now has the
highest degree of polarisation of the day, reaching between 70% and 80%
polarisation (Brines and Gould,
1982; Wehner,
1989
). This high degree of polarization stretches in a band across
the sky from south to north. The remainder of the skylight is polarised in a
parallel direction with falling degrees of polarisation towards the sun and
the anti-sun. On nights with a full moon, a similar pattern of polarised light
will also form around this source of light
(Gál et al., 2001
).
In the compound eyes of beetles and other arthropods, the microvilli of the
retinula cells form light-absorbing rhabdoms. In polarisation-sensitive
insects, the arrangement of these structures follows a common pattern; the
microvilli in each rhabdomere are organised in only one of two orthogonal
directions (for a review, see Labhart and
Meyer, 1999). With a maximum sensitivity to light polarised
parallel to the direction of the microvilli
(Goldsmith and Wehner, 1977
;
Hardie, 1984
;
Israelachvili and Wilson,
1976
), this arrangement tunes the two groups of receptors to
orthogonal planes of polarisation. An opponency between the two sets of
receptors will not only enhance the polarisation contrast but will also make
the system independent of the light intensity of the stimulus
(Labhart, 1988
;
Nilsson and Warrant, 1999
).
This rhabdom design is generally confined to a narrow strip at the dorsal rim
of the eye, termed the dorsal rim area (DRA;
Labhart, 1980
). Within this
area, there are often additional specialisations to facilitate the perception
of the polarised light in the sky. Examples of such are a lack of screening
pigments or poor lens optics (Aepli et al.,
1985
; Burghause,
1979
; Labhart et al.,
1992
; Meyer and Labhart,
1981
,
1993
;
Ukhanov et al., 1996
).
As the day slips towards night, many animals begin or end
their activity. The dung beetle Scarabaeus zambesianus starts to fly
at around sunset with the prospect of finding fresh dung. Once found, it forms
a ball of dung and rolls it off at high speed in a line as straight as the
terrain will allow. This is supposedly done to avoid competition at and around
the food source. The ball is finally buried in a suitable place to be consumed
in secure solitude, either by the beetle itself or by a beetle larva
(Hanski and Cambefort, 1991).
While rolling, the beetle inevitably has to rely upon some sort of reference
to stay on route. For many animals, this cue is the polarisation pattern of
skylight, a stimulus well known to be used for orientation (see
Waterman, 1981
).
Whereas diurnal polarised light orientation has been thoroughly explored,
twilight orientation remains a rarely investigated topic. An exception is the
use of skylight polarization in dusk-migrating birds (Helbig,
1990,
1991
;
Moore and Philips, 1988
;
Philips and Moore, 1992), cockchafers
(Labhart et al., 1992
) and
spiders (Dacke et al., 1999
,
2001
). The mechanism behind the
perception of polarised light in birds, however, remains unsolved, and some
studies even argue against a use of skylight polarisation as a cue
(Coemans et al., 1994
).
Dusk-active bumblebees have also been suggested to navigate using the
polarised light pattern at dusk, when the surroundings are too dim to
distinguish terrestrial landmarks
(Wellington, 1974
). The
morphological basis of this behaviour has, to our knowledge, not yet been
investigated.
In the present study, we combine the results of behavioural studies of polarised light orientation in the field with those of morphological studies of the eyes of the crepuscular dung beetle Scarabaeus zambesianus. By restricting our experiments to moonless evenings, the beetles could only use direct sunlight and the polarized light pattern of skylight for celestial orientation. We show that polarised light in the sky is used by beetles for orientation to roll balls in straight paths, and we identify the receptors used to perceive this skylight cue. Based on these results, we also question whether the fan-shaped arrangement of analysers in the DRA is an adaptation to polarised light orientation.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Polarised light navigation
In a simple set of experiments, the beetles were allowed to roll along
their chosen course with an undisturbed view of the evening sky. A
semitransparent Perspex barrier (7 cm high x 30 cm wide) was placed
perpendicular to the path of the beetle, forcing the beetle to move around it.
The deviation after the obstacle, from the path taken before the obstacle, was
measured with a protractor using the tracks made by the beetles in the fine
sand as indicators of the path. All measurements were taken within the first
hour after sunset on moonless nights.
In a second experiment, a polarising filter (Polaroid HN 22) with a circular diameter of 42 cm was mounted in a holder with four symmetrically placed legs, each with a height of 10 cm. With the help of a magnetic compass fitted on the holder, the filter was placed under the open sky over the expected path of the beetle with its e-vector transmission axis oriented in a west-easterly direction (Fig. 1). Thus, as the beetle entered the area below the filter, the south-northerly oriented polarised light pattern of evening skylight appeared to switch by 90°. The exact orientation of the filter had to be adjusted according to the azimuth of the setting sun. In our experiments, the sun set at 250° east of north and the transmission axis of the filter was oriented 70250° east of north to simulate a 90° switch of the polarised twilight pattern of skylight. The reaction of the beetles to this switch was filmed using a Sony video camera equipped with `night-shot' and was later analysed in the laboratory for tracing the path of the beetle. Both the empty holder and the holder with the filter with its e-vector transmission axis oriented in a south-northerly direction were placed over the expected path of the beetle to act as two controls. The reaction of the beetles to these controls was recorded and analysed as described above.
|
In the laboratory, we used the same filter and holder as described above, but the filter was now rotated within the holder. An Osram Ultra-Vitalux lamp (300 W) was used as a light source, centred above the filter. Tracing paper was placed on top of the polarising filter to present an extended polarised stimulus. A beetle and its ball were placed in an arena (70 cmx100 cm) covered with fine sand. As soon as the beetle had rolled 5 cm in under the filter, the filter was rotated through 90°. The angle turned by the beetle, in response to the filter being turned, was measured by analysing the track made by the beetle in the fine sand. As a control, the track made by the beetles under a stationary filter was also recorded. The direction taken towards the centre of the filter was compared with the direction taken after this point.
Histology
Sections for light and electron microscopy were prepared using conventional
techniques. The eyes were dissected and fixed for 72 h at 8° in a fixative
containing 2.5% glutaraldehyde, 2% paraformaldehyde and 0.1 mmol
l1 EGTA in 0.1 mol l1 cacodylate buffer.
The buffer was adjusted to pH 7.2. Following postfixation with 1%
OsO4 in 0.1 mol l1 cacodylate buffer for 2.5 h at
room temperature, the tissue was dehydrated in an ethanol and propylene oxide
series and embedded in Epon resin. A possible twist of the DRA rhabdoms was
analysed by 0.5 µm cross-sections through the depth of the DRA. In these
sections, a single rhabdom was identified during sectioning with the help of
irregularities in the retina. The orientation of the transverse-axis of this
rhabdom and neighbouring rhabdoms was determined every five sections.
Ultra-thin sections (50 nm) were taken and prepared for electron microscopy
with 1% uranyl acetate and lead citrate. Animals used for scanning electron
microscopy were air-dried and sputter coated with goldpalladium
(40/60).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
General behaviour
S. zambesianus starts forming a ball of dung immediately after
landing on a pile of fresh dung. It does so by the use if its flat front legs.
As soon as the ball is ready, the beetle pushes it off the pile and climbs on
top of it. Here, it cleans its eyes, stretches its head out and performs one
or two rotatory (yaw) body movements before it climbs down and starts rolling,
head down, pushing the ball with its hind legs. If the beetle encounters a
branch or a deep hole that makes it fall over, it often repeats its little
dance on top of the ball before it starts rolling again. The ball is finally
buried at a suitable spot some 530 m away. All balls rolled in this
study were feeding balls to be consumed by the beetle itself. Once the ball of
dung is depleted, the beetle will leave the burial spot never to return
again.
Orientation to polarised light
With a full view of the moonless twilight sky, the beetles (N=15)
negotiate an obstacle placed in their way by continuously pushing the ball
sideways. As they reach the end of the obstacle they again set out parallel to
the course they started with an absolute mean angular deviation from the
original running direction of 16.9±11.5° (mean ± S.D.). Of
15 beetles, seven turned to the left from the original running direction and
eight turned to the right (Fig.
2). Taking the directions of the deviations into consideration,
where a left turn is assigned a `minus' and a right turn is assigned a `plus',
there is no bias to the left or to the right (0.2±20.3°).
This experiment clearly shows that, in general, beetles maintain their chosen
course, deviating from it only temporarily when forced to do so.
|
In the second experiment, the natural polarisation pattern was manipulated via rotation by 90° as beetles (N=26) rolled their ball in under a polarising filter. The beetles continued to roll along their chosen course until they were at least 5 cm in under the filter. Without any delay, they then turned in response to the rotated polarisation pattern (Fig. 1). A mean turn of 80.9±15.8° was close to the expected 90°. A small turn of 6.7±5.0°, recorded in response to rolling in under a polarising filter placed with its e-vector transmission axis oriented parallel to the e-vector of evening skylight, was not significantly different (t-test, P>0.05) from the response when rolling in under the empty holder of the filter (4.6±4.5°).
In the laboratory, where the beetles (N=8) were exposed to a polarising filter rotated through 90°, the turn was smaller, with a mean value of 61.4±16.1°. With a non-rotated filter, no turn was recorded.
Morphology of the eye and standard ommatidia
The eyes of S. zambesianus are divided into dorsal and ventral
eyes by a cuticular ridge, the canthus, which projects from the edge of the
`cheek' (Fig. 3). The dorsal
eye is the smaller of the two. Each of these eyes acts independently as a
superposition eye. The surface of the eye is perfectly smooth without any
visible facets. The thick corneal lens of each ommatidium is attached to a
crystalline cone, beneath which is a clear zone and a 120 µm-long rhabdom.
No screening pigments, but a tracheal tapetum, can be found between the
rhabdoms as far as half way up the rhabdom. For the structures mentioned
above, no differences were observed among different regions from the dorsal
and ventral eyes. Microvilli from seven of eight retinula cells form the
rhabdom in both eyes, but the arrangement of these structures varies across
the eye. In the ventral eye and the ventral half of the dorsal eye, the
microvilli form a flower-shaped rhabdom
(Fig. 4B,C). Here, the
microvilli run in different directions in different rhabdomeres.
|
|
Specialised ommatidia of the dorsal rim area
In the dorsal half of the dorsal eyes, the microvilli of the seven cells
run in only two directions, forming an almost heart-shaped structure in
cross-section (Figs 4A,
5). In these specialised
ommatidia, the microvilli of receptor cell 1 run parallel to those of cell 1
in neighbouring ommatidia but perpendicular to the microvilli of the remaining
cells (27) of the ommatidium (for cell numbering, see
Labhart et al., 1992). This
special eye region, termed the dorsal rim area (DRA;
Labhart 1980
), extends for
approximately 26 ommatidia along the dorsal rim of the eye. With a width of
approximately 20 ommatidia in the centre, narrowing towards the ends, the DRA
covers roughly 50% of the dorsal eye (Fig.
3A). Serial cross-sectioning through the entire length of the
rhabdoms indicates that there is no rhabdomeric twist or big jumps in
microvillar orientation. Microvillar misalignment strongly influences the
polarisation sensitivity as it make the retinula cell less sensitive to one
single direction of polarisation (Nilsson
et al., 1987
; Wehner et al.,
1975
). The transvere-axis of the DRA rhabdoms, defined by the
microvillar direction of photoreceptor cells 27, is oriented in a
dorsally converging fan-shaped pattern across the eye
(Fig. 5). The border of the DRA
can easily be found based on the changing appearance of the rhabdoms, but no
sharp border can be seen in the orientation of the ommatidial rows. The
flower-shaped rhabdoms in the remainder of the eye simply seem to follow the
same orientation scheme as in the DRA (Fig.
5).
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Orientation to polarised light
For an animal active shortly after sunset, the visual cues that can be used
for orientation are fairly limited. It is just dark enough for the stars to be
visible and the moon is not always present. Terrestrial landmarks might be
used but they will be hard to detect at these low light levels. The only cues
left are the polarised light pattern present in the sky together with a
brighter sky towards the setting sun. When the direction of the pattern of
polarised skylight was artificially switched by 90°, the beetle
accordingly changed its course. The same response, but less pronounced, can
also be observed in the laboratory. The somewhat smaller turn of the beetle in
the laboratory is likely to be explained by a decreased desire to roll when
kept in captivity. Nevertheless, both experiments clearly indicate that the
beetles perceive the e-vector of light and use it to roll their balls along a
chosen path.
In the field, a polarising filter will artificially change the intensity of
the skylight polarisation pattern. When the filter is placed with its e-vector
transmission axis perpendicular to the dominant polarisation direction of
skylight at dusk (northsouth), the darkest part of the sky will now be
perceived from the zenith (where the degree of polarisation is the highest)
rather than from the east. West, however, will still remain the brightest part
of the sky and could still serve as a compass cue for orientation. The
recorded turn of the beetles under the filter thus shows that polarised light
could well be the primary cue used by the beetle to maintain its bearing. The
little dance performed on the top of the ball before S. zambesianus
starts to roll supports this idea. In other navigating insects, such rotations
are believed to recalibrate the polarization compass before they start their
journey (Wehner, 1997).
A course-stabilising function of polarisation vision has also been
suggested in flies (von Philipsborn and
Labhart, 1990; Wellington,
1953
; Wolf et al.,
1980
; Wunderer and Smola,
1982
) and crickets (Brunner and
Labhart, 1987
). Common to these insects, and most other
polarisation-sensitive insects, is that the receptors used for celestial
polarisation analysis are restricted to the DRA of the eye
(Labhart and Meyer, 1999
).
This also holds true for S. zambesianus.
A DRA for polarised light detection
The location of the DRA is revealed by the shape of the rhabdoms. The two
sets of receptors with parallel microvilli, oriented 90° to each other,
can be found only in the rhabdoms within this dorsal area and these well
satisfy the requirements for a polarisation opponent analyzer. A second
important characteristic for high polarisation sensitivity is that the
microvilli are well aligned along the length of the rhabdom
(Nilsson et al., 1987;
Wehner et al., 1975
).
In some animals, the location of the DRA can be observed from the surface
of the eye. Light-scattering cavities in the cornea, or differently shaped
facets, discriminate this area from the rest of the eye
(Aepli et al., 1985;
Burghause, 1979
;
Labhart et al., 1992
;
Meyer and Labhart, 1981
;
Ukhanov et al., 1996
). No such
differences can be found in the cornea or are visible on the smooth, glassy
surface of the eye in S. zambesianus; neither has it been reported in
the dung beetle P. striatum
(Dacke et al., 2002
) or in any
other morphological study of the eyes of dung beetles (Scarabaeidae) where an
ability to detect the polarisation of light has been suggested (Gokan,
1989a
,b
,c
,
1990
;
Gokan and Meyer-Rochow, 1990
;
Meyer-Rochow, 1978
).
Light-scattering cavities, or differently shaped facets to aid in polarised
light detection, thus appear to be absent within the dung beetles
(Scarabaeidae).
Adaptations for polarised light detection at low light levels
For polarised light orientation around sunset, the sensitivity of the
detector becomes more and more critical as light levels fall continuously with
the setting sun. Low light intensities will become a problem for the whole
visual system, but here we focus our interest only on the DRA. The dung beetle
P. striatum is also able to orient to polarised skylight but is
active during the day in one of the brightest habitats on earth: the
sun-flooded desert plain (Dacke et al.,
2002; Scholtz,
1989
). How does the optical sensitivity of the DRA in S.
zambesianus compare with that in this day-navigating species?
The difference between the two species becomes obvious upon comparison of
the rhabdoms from the DRA (Fig.
7; Table 1). The
rhabdom in S. zambesianus is both much longer and almost three times
as wide as that in P. striatum. This allows the receptors of S.
zambesianus to collect more light and, thus, makes them more sensitive
(Land, 1981). In addition, the
tracheal tapetum of S. zambesianus reflects light back through the
rhabdom a second time, effectively making the rhabdom twice as long. An
estimate of how much more sensitive the DRA in S. zambesianus is can
be obtained by calculating its optical sensitivity, S, to an extended
source of light (Kirschfeld,
1974
; Land, 1981
,
1989
; modified for white light
by Warrant and Nilsson, 1998
):
![]() | (1) |
|
|
Do the beetles stop foraging when they can no longer perceive and orient to
the e-vector of light? At this point, we can only hypothesise about whether
this is the case. On a moonless night, the beetles cease their activity
4050 min after sunset. This halt in activity coincides with the time of
night when the light intensity drops dramatically and the degree of
polarisation at the sky's zenith decreases from 45% to 5% within 15 min
(Dave and Ramanathan, 1956).
Crickets can detect the e-vector of strongly polarised light at intensities
that are even lower than that from a clear moonless sky, and during the day
they need no more than 5% polarisation to detect the direction of polarisation
(Herzmann and Labhart, 1989
;
Labhart, 1996
). For S.
zambesianus, low light intensities will unfortunately coincide with low
degrees of polarisation, and the critical threshold for orientation to the
polarisation of twilight skylight will thus probably occur at higher
intensities and degrees of polarisation than those recorded for crickets. On
moonlit nights, the beetles stay active longer than on moonless nights,
possibly using the moon as an orientation source when the polarised light
pattern from the sun is no longer available.
A fan-shaped pattern of the analysers is a consequence of the
ontogeny of the eye
S. zambesianus has the same ommatidial array as that found in the
DRA of all diurnal (Burghause,
1979; Dacke et al.,
2002
; Wehner,
1982
; Wunderer and Smola,
1982
) and crepuscular (Labhart
et al., 1992
) animals where this has been carefully mapped. This
arrangement is remarkably stable between different insect groups, irrespective
of whether they have superposition or apposition eyes. It is also stable
between insects orienting to the polarisation of skylight at different times
of the day. About 15 years ago, this fan-shaped arrangement of the ommatidial
axis in the DRA was proposed to mimic the e-vector pattern of skylight
(Wehner 1989
), but even then
the possibility was raised that the arrangement could be a natural consequence
of the spherical shape of the eye. In S. zambesianus, we found no
morphological difference in the arrangement of the ommatidial rows in the DRA
from that in the rest of the eye. This supports the idea that the arrangement
of the rhabdoms in the DRA is simply a consequence of the way the eye is
built, rather than an adaptation to polarised light analysis. Adaptations for
polarised light detection are more likely restricted to the optics of the eye,
the orthogonal arrangement of the microvilli and in the way in which the
signals from the polarisation analysers are pooled
(Blum and Labhart, 2000
;
Labhart et al., 2001
).
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Aepli, F., Labhart, T. and Meyer, E. P. (1985). Structural specializations of the cornea and retina at the dorsal rim of the compound eye in hymenopteran insect. Cell. Tissue Res. 239, 19-24.
Blum, M. and Labhart, T. (2000). Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye. J. Comp. Physiol. A 186,119 -128.[CrossRef][Medline]
Brines, M. L. and Gould, J. L. (1982). Skylight polarisation patterns and animal orientation. J. Exp. Biol. 96,69 -91.
Brunner, D. and Labhart, T. (1987). Behavioural evidence for polarization vision in crickets. Physiol. Entomol. 12,1 -10.
Bruno, M. S., Barnes, S. N. and Goldsmith, T. H. (1977). The visual pigment and visual cycle of the lobster Homarus. J. Comp. Physiol. 120,123 -142.
Burghause, F. M. H. R. (1979). Die strukturelle Spezialisierung des dorsalen Agentteils der Grillen (Orthoptera, Grylloidea). Zool. Jb. Physiol. 83,502 -525.
Coemans, M. A. J. M., Vos Hzn, J. J. and Nuboer, J. F. W.
(1994). The orientation of the E-vector or linearly polarized
light does not affect the behavior of the pigeon Columbia livia. J.
Exp. Biol. 191,107
-123.
Dacke, M., Nilsson, D.-E., Warrant, E. J., Blest, A. D., Land, M. F. and O'Carroll, D. C. (1999). Built-in polarizers form part of a compass organ in spiders. Nature 401,470 -473.[CrossRef]
Dacke, M., Doan, T. A. and O'Carroll, D. C. (2001). Polarized light detection in spiders. J. Exp. Biol. 204,2481 -2490.[Medline]
Dacke, M., Nordstöm, P., Scholtz, C. H. and Warrant, E. J. (2002). A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle Pachysoma striatum.J. Comp. Physiol. A 188,211 -216.[CrossRef]
Dave, J. V. and Ramanathan, K. R. (1956). On the intensity and polarisation of the light from the sky during twilight. Proc. Indian Acad. Sci. 43A, 67-68.
Frantsevich, L., Govardovsky, V., Gribakin, F., Nikolajev, G., Pichka, V., Polanovsky, A., Shevchenko, V. and Zolotov, V. (1977). Astroorientation in Lethrus (Coleoptera, Scarabaeidae). J. Comp. Physiol. 121,253 -271.
Gál, J., Horváth, G., Barta, A. and Wehner, R. (2001). Polarization of the moonlit clear night sky measured by full-sky imaging polarimetry at full moon: comparison of the polarization of moonlit and sunlit skies. J. Geophys. Res. 106,22647 -22653.
Gokan, N. (1989a). Fine structure of the compound eye of the dung beetle Ochodaeus maculatus (Coleoptera, Scarabaeidae). Jpn. J. Ent. 57,823 -830.
Gokan, N. (1989b). Fine structure of the compound eye of the dung beetle Aphodius haroldianus (Coleoptera: Scarabaeidae). Appl. Ent. Zool. 24,483 -486.
Gokan, N. (1989c). The compound eye of the dung beetle Geotrupes auratus (Coleoptera: Scarabaeidae). Appl. Ent. Zool. 24,133 -146.
Gokan, N. (1990). Fine structure of the compound eye of the dung beetle Onthophagus lenzii (Coleoptera, Scarabaeidae). Jpn. J. Ent. 58,185 -195.
Gokan, N. and Meyer-Rochow, V. B. (1990). The compound eye of the dung beetle, Onthophagus posticus (Coleoptera: Scarabaeidae). N. Z. Ent. 13, 7-15.
Goldsmith, T. H. and Wehner, R. (1977). Restrictions on rotational and translational diffusion of pigment in the membranes of a rhabdomeric photoreceptor. J. Gen. Physiol. 70,453 -490.[Abstract]
Hanski, I. and Cambefort, Y. (1991). Dung Beetle Ecology. Princeton, NJ: Princeton University Press.
Hardie, R. C. (1984). Properties of photoreceptors R7 and R8 in dorsal marginal ommatidia in the compound eyes of Musca and Calliphora. J. Comp. Physiol. A 154,157 -165.
Helbig, A. J. (1990). Depolarization of natural skylight disrupts orientation of an avian nocturnal migrant. Experientia 46,755 -758.
Helbig, A. J. (1991). Dusk orientation of migratory European robins, Erithacus rubecula: the role of sunrelated directional information. Anim. Behav. 41,313 -322.
Herzmann, D. and Labhart, T. (1989). Spectral sensitivity and absolute threshold of polarization vision in crickets: a behavioral study. J. Comp. Physiol. A 165,315 -319.
Israelachvili, J. N. and Wilson, M. (1976). Absorption characteristics of oriented photopigments in microvilli. Biol. Cybern. 21,9 -15.[Medline]
Kirschfeld, K. (1974). The absolute sensitivity of lens and compound eyes. Z. Naturforsch. (C) 29,592 -596.
Labhart, T. (1980). Specialized photoreceptors at the dorsal rim of the honeybee's compound eye: polarizational and angular sensitivty. J. Comp. Physiol. 141, 19-30.
Labhart, T. (1988). Polarization-opponent interneurons in the insect visual system. Nature 331,435 -437.
Labhart, T. (1996). How polarization-sensitive
interneurones of crickets perform at low degrees of polarization.
J. Exp. Biol. 199,1467
-1475.
Labhart, T. and Meyer, E. P. (1999). Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc. Res. Tech. 47,368 -379.[CrossRef][Medline]
Labhart, T., Meyer, E. P. and Schenker, L. (1992). Specialized ommatidia for polarization vision in the compound eye of cockchafers, Melolontha melolontha (Coleoptera, Scarabaeidae). Cell. Tissue Res. 268,419 -429.[Medline]
Labhart, T., Petzold, P. and Helbling, H. (2001). Spatial integration in polarization-sensitive interneurones of crickets: a survey of evidence, mechanisms and benefits. J. Exp. Biol. 204,2423 -2430.[Medline]
Land, M. F. (1981). Optics and vision in invertebrates. In Handbook of Sensory Physiology, vol.VII/6B (ed. H. Autrum), pp.471 -592. Berlin, Heidelberg, New York: Springer Verlag.
Land, M. F. (1989). Variations in the structure and design of compound eyes. In Facets of Vision (ed. D. G. Stavenga and R. C. Hardie), pp. 90-111. Berlin, Heidelberg: Springer Verlag.
McIntyre, P. D. and Caveney, S. (1998). Superposition optics and the time of flight in onitine dung beetles. J. Comp. Physiol. A 183,45 -60.[CrossRef]
Meyer, E. P. and Labhart, T. (1981). Pore canals in the cornea of a functionally specialized area of the honey bee's compound eye. Cell. Tissue Res. 216,491 -501.[Medline]
Meyer, E. P. and Labhart, T. (1993). Morphological specializations of dorsal rim ommatidia in the compound eye of dragonflies and damselflies (Odonata). Cell. Tissue Res. 272,17 -22.
Meyer-Rochow, V. B. (1978). Retina and dioptic apparatus of the dung beetle Euonticellus africanus. J. Insect. Physiol. 24,165 -179.
Moore, F. R. and Philips, J. B. (1988). Sunset, skylight polarization and the migratory orientation of yellowrumped warblers, Dendroica coronata. Anim. Behav. 36,1770 -1778.
Müller, M. and Wehner, R. (1988). Path integration in desert ants, Cataglyphis fortis. Proc. Natl. Acad. Sci. USA 85,5287 -5290.[Abstract]
Nilsson, D.-E. and Warrant, E. J. (1999). Visual discrimination: seeing the third quality of light. Curr. Biol. 9,R535 -R537.[CrossRef][Medline]
Nilsson, D., Labhart, T. and Meyer, E. P. (1987). Photoreceptor design and optical properties affecting polarization sensitivity in ants and crickets. J. Comp. Physiol. A 161,645 -658.
Phillips, J. B. and Moore, F. R. (1992). Calibration of the sun compass by sunset polarized light patterns in a migratory bird. Behav. Ecol. Sociobiol. 31,189 -193.
Rozenberg, G. V. (1966). Twilight: a Study in Atmospheric Optics. New York: Plenum Press.
Schmidt, I., Collett, T. S., Dillier, F.-X. and Wehner, R. (1992). How desert ants cope with enforced detours on their way home. J. Comp. Physiol. A 171,285 -288.
Scholtz, C. H. (1989). Unique foraging behaviour in Pachysoma (= Scarabaeus) striatum Castelnau (Coleoptera:Scarabaeidae): an adaptation to arid conditions? J. Arid Env. 16,305 -313.
Ukhanov, K., Leertouwer, H. L., Gribakin, F. G. and Stavenga, D. G. (1996). Dioptrics of the facet lenses in the dorsal rim area of the cricket Gryllus bimaculatus. J. Comp. Physiol. A 179,545 -552.
von Philipsborn, A. and Labhart, T. (1990). A behavioural study of polarization vision in the fly, Musca domestica.J. Comp. Physiol. A 167,737 -743.
Warrant, E. J. and McIntyre, P. D. (1991). Strategies for retinal design in arthropod eyes of low F-number. J. Comp. Physiol. A 168,499 -512.
Warrant, E. J. and Nilsson, D.-E. (1998). Absorption in of white light in photoreceptors. Vision Res. 38,195 -207.[CrossRef][Medline]
Waterman, T. H. (1981). Polarization sensitivity. In Handbook of Sensory Physiology, vol.VII/6B (ed. H. Autrum), pp.281 -469. Berlin, Heidelberg, New York: Springer Verlag.
Wehner, R. (1982). Himmelsnavigation bei Insekten. Neurophysiologie und Verhalten. Neujahrsbl. Naturforsch. Ges. Zürich 184,1 -132.
Wehner, R. (1989). The hymenopteran skylight compass: matched filtering and parallel coding. J. Exp. Biol. 146,63 -85.
Wehner, R. (1997). The ant's celestial compass system: spectral and polarization channels. In Orientation and Communication in Arthropods (ed. M. Lehrer), pp.145 -185. Basel: Birkhäuser Verlag.
Wehner, R. and Wehner, S. (1986). Path integration in desert ants. Approaching a long standing puzzle in insect navigation. Monitore Zool. Ital. 20,309 -331.
Wehner, R., Bernard, G. D. and Geiger, E. (1975). Twisted and non-twisted rhabdoms and their significance for polarization detection in the bee. J. Comp. Physiol. 104,225 -245.
Wellington, W. G. (1953). Motor responses evoked by the dorsal ocelli of Sarcophaga aldrichi Parker, and the orientation of the fly to plane polarized light. Nature 172,1177 -1179.[Medline]
Wellington, W. G. (1974). Bumblebee ocelli and navigation at dusk. Science 183,550 -551.
Wolf, R., Gerbhardt, B., Gademann, R. and Heisenberg, M. (1980). Polarization sensitivity of course control in Drosophila melanogaster. J. Comp. Physiol. 139,177 -191.
Wunderer, H. and Smola, U. (1982). Fine structure of ommatidia at the dorsal eye margin of Calliphora erythrocephala Meigen (Diptera: Calliphoridae): An eye region specialised for the detection of polarized light. Int. J. Insect Morphol. Embryol. 11,25 -38.