Interindividual variation of eye optics and single object resolution in bumblebees
Zoologie II, Biozentrum, University of Würzburg, Am Hubland, 97074 Würzburg, Germany
Author for correspondence at present address: School of Biological Sciences,
Queen Mary, University of London, Mile End Road, E1 4NS, UK (e-mail:
l.chittka{at}qmul.ac.uk)
Accepted 25 June 2003
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Summary |
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Key words: compound eye, detection, facet, ommatidium, visual ecology, bumblebee, Bombus terrestris
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Introduction |
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Thus, behavioural tests must be combined with quantifications of eye optics
to determine how target detection ability varies with body size. Here, we
employ a size-polymorphic insect species, the bumblebee Bombus
terrestris, to determine this relationship quantitatively. There are
numerous studies to show that the optical properties of complex eyes are
scaled with body size (Land,
1981; Snyder and Menzel,
1975
) both within (Zollikofer
et al., 1995
) and across species
(Jander and Jander, 2002
).
Larger animals tend to have more ommatidia per eye, larger facets (and hence
higher overall sensitivity) and smaller interommatidial angles, resulting in
higher visual resolution (Jander and
Jander, 2002
; Wehner,
1981
; Zollikofer et al.,
1995
). But can we extrapolate directly from eye optics to
behavioural ability at target detection? There are behavioural studies to
determine the minimal detectable size of visual targets or, alternatively, the
minimum grating resolution across a range of insects
(Baumgärtner, 1928
;
Gould, 1988
;
Lehrer and Bischof, 1995
;
Macuda et al., 2001
;
Rutowski et al., 2001
;
Vallet and Coles, 1991
). But
the experimental conditions and behavioural contexts are too heterogeneous
across studies to reveal a consistent picture.
Bumblebees are an ideal species to quantify the relationship between body
size, eye optics and behavioural ability at visual stimulus detection. They
exhibit a pronounced size polymorphism: workers of a single colony can differ
in body mass by a factor of 10, which is unique in the social bees
(Michener, 1974). We quantify
the optics of the eyes of Bombus terrestris workers over a wide range
of sizes, and their relationship with the ability to detect artificial
flowers.
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Materials and methods |
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Scanning electron microscopy (SEM)
For estimating ommatidial number and diameter, we removed the left eyes of
freshly killed bees with a razor blade and glued them with their inner side on
an SEM table. Eyes were air-dried, gold-palladium coated (Balzers sputter
coater SCD 005; Bal-Tec, Balzers, Switzerland) and viewed with a scanning
electron microscope (Zeiss DSM 962; Jena, Germany). On the SEM photos, we
marked a 1 mm2 area in the centre of each eye and counted all
ommatidia inside this area. Of 15 randomly selected ommatidia, we measured
facet diameter (tip-to-tip distance of the hexagonal lens). We scanned the
photos of each eye into a computer and measured eye surface area using an
imaging program (Scion image; Scion corporation, Frederick, MA, USA). The
number of ommatidia per eye was calculated by counting ommatidia per 1
mm2 multiplied by eye surface area. Note that this provides an
underestimate of total ommatidial number because, in bees, the largest lenses
are found in the centre of the eye, where we performed our measurements.
Ommatidial size decreases systematically as one moves to the periphery
(Jander and Jander, 2002).
However, the ratio of facet diameters between the centre and the (dorsal)
margin of the eye appears to be nearly constant over a wide range of diurnal
bee species with different sized individuals
(Jander and Jander, 2002
).
Therefore, it is unlikely that our estimates bias the qualitative relationship
between eye size and facet number.
Optical axes of ommatidia
We determined the divergence angle between two ommatidia by examining the
pseudopupils under antidromic illumination conditions
(Seidl and Kaiser, 1981;
Snyder et al., 1977
). As
described by Seidl and Kaiser
(1981
; see their
fig. 1), we glued the head of a
bumblebee onto the tip of a light guide (
=1 mm) and mounted it in the
centre of a perimeter apparatus, connected to a microscope. We adjusted the
head of the bee so that we could see the bright corneal pseudopupils that
result from light emitted from the distal tips of the rhabdoms in the
medial-frontal part of the compound eye. We evaluated this eye region because
it is the one used for target detection in our behavioural tests. We measured
the distance between the light beams radiating from the facets at the corneal
surface and at a 500 µm distance from the surface by means of a camera
lucida connected to the microscope (Axiophot; Zeiss). We focused the
microscope first on the eye surface, marked the pseudopupils, moved the focal
plane 500 µm above the surface and marked the pseudopupils again. From
these data, we calculated the divergence angles in the horizontal
(
h) and vertical (
v) plane
according to:
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Behavioural tests
Bumblebee colonies were connected to a flight cage (0.45 m x 0.45 m;
0.3 m height; Fig. 2A)
via a Plexiglas tube. Shutters between the nest and the arena allowed
us to control access of selected workers. The arena had the shape of a
Y-maze with an entrance chamber and two tunnels (0.3 m width x
0.2 m length x 0.3 m height) branching from a trilateral decision
chamber (0.3 m x 0.3 m x 0.42 m; 0.3 m height). The two back walls
of the tunnels consisted of white plastic boards (0.3 m x 0.3 m) with a
central hole (1 cm ). Behind each hole, a small plastic tube with
sucrose solution could be attached. The arena was covered by a UV-transmitting
Plexiglas top. The targets (`flowers') were yellow paper disks of
=15.9, 7.9, 5.5, 3.9, 3.1, 2.4 or 1.6 cm, presented on a white
background. The spectral reflectance of the target and background (see
Fig. 3) was measured by means
of a spectrometer (S2000 spectrometer with a deuterium/halogen light source;
Ocean Optics, Dunedin, FL, USA). The relative amount of light (P)
absorbed by the bees' spectral receptors is determined by:
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The green contrast between target and background in our set-up was 0.11,
where maximum green contrast is 0.5
(Spaethe et al., 2001). This
is because, by definition, for the adaptation background E equals 0.5
in each photoreceptor. Green contrast, then, is the degree to which any given
stimulus generates an excitation value different from 0.5 in the green
receptor. Because excitation can range from 0 to 1, the maximum green contrast
is 0.5.
This means that, in our target, green contrast is strong and is well above
detection threshold (Giurfa et al.,
1996). This is important because the green receptor channel limits
spatial resolving power in bees
(Srinivasan and Lehrer, 1988
)
- if a target differs from its background only in the UV or blue receptor
signals, spatial resolution is substantially worse. This is because bees will
then resort to using colour contrast, which requires that a target subtends
15° (Giurfa et al., 1996
;
Giurfa and Lehrer, 2001
).
Colour contrast between target and background was 0.301; brightness contrast,
given as the difference in sum of the three photoreceptor type signals, is
0.912.
The visual angle () of the target was calculated by
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Number of ommatidia involved in target detection
The bumblebee eye is oval. Therefore, a circular stimulus, as used in our
experiment, excites the ommatidia within an oval area of the eye surface. The
determination of the minimal number of ommatidia involved in target detection
is not simple, however. This is because the axes of the ommatidia point in
slightly different directions and have roughly Gaussian (rather than simple
step-wise) angular sensitivities (Vorobyev
et al., 1997). Some will receive light reflected from both the
target and the background. Thus, the excitation (E) of a certain
ommatidium by the stimulus at a certain visual angle is affected by both the
inclination of the ommatidial axis with respect to the stimulus (determined by
the angle between neighbouring ommatidia,
) and its visual field,
measured as acceptance angle (
). We determined the excitation of
an ommatidium by a stimulus by integrating the angular sensitivity function,
A(
h,
v), of the ommatidium over the
area of the target:
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![]() | (9) |
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Results |
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We found that interommatidial angles in the medial-frontal part of the eye decrease with increasing body size (Fig. 5), both in the vertical (from 0.6° to 1.4°; Spearman's rank correlation rs=-0.52, P=0.041, N=16) and the horizontal (from 1.8° to 3.3°; rs=-0.69, P=0.003, N=16) dimension. An increase in body size (thorax width) by a factor of 1.5 is accompanied by a 32% reduction of the divergence angles in the vertical dimension and a 19% reduction in the horizontal dimension. In conclusion, large bees combine the advantage of larger facet diameters (lower diffraction, higher overall sensitivity) with the benefit of lower interommatidial angles (more fine-grained picture). They should therefore have higher visual resolving power.
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Single object resolution
Our results show that the gains associated with an increase in body size
(and the predicted improvement in visuo-spatial resolving power) are
significant. We found a significant negative correlation between the minimum
visual angle at which a stimulus can be detected and the size of the bumblebee
(rs=-0.73, P=0.01, N=11). For example, a
large bee (4.7 mm thorax width) can detect objects of half the size that a
small bee (3.5 mm thorax width) can from the same distance
(Fig. 2B). Large bumblebee
workers also exhibit much better visual resolution than honeybees (minimum
visual angle of 3.5° vs 5°), whereas small bumblebees perform
worse (7° minimum visual angle). Qualitatively, the observed correlation
is unsurprising, but can behavioural detection ability be
quantitatively predicted from eye optics alone? To answer this
question, we must calculate the number of ommatidia actually involved in
detection for workers of different sizes.
Number of ommatidia involved in target detection
The number of ommatidia involved in object detection varies between
individuals and correlates with worker size
(Fig. 6). In small bees (thorax
width <3.5 mm), excitation of seven ommatidia is required for stimulus
detection; the same number that was determined in the honeybee
(Giurfa et al., 1996). Over a
range of intermediate sizes (3.5-4.3 mm), the number of ommatidia that need to
be excited for target detection is three. In large workers (>4.3 mm), only
a single ommatidium is necessary for reliable detection of a coloured object.
(Note that there are no body sizes for which we predict a minimal ommatidia
number of 2, 4 or 6, because the minimal area expands in the horizontal and
vertical directions symmetrically as a function of body size.)
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Discussion |
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These estimates are based on the acceptance angle from honeybee ommatidia,
as quantified by Laughlin and Horridge
(1971). The lens diameter in
the frontal eye is similar between honeybees (21.6 µm;
Barlow, 1952
) and our smallest
worker (19.5 µm). It is likely that larger bumblebees have ommatidia with
smaller acceptance angles due to larger lens diameters
(Warrant and McIntyre, 1993
).
Taking this into account, the superscript in equation 9 would be additionally
reduced in larger bees, which might result in an even stronger reduction of
the ommatidial array stimulated as shown in
Fig. 6 for large workers. Thus,
our estimate is conservative.
There are two possible interpretations for our findings. One possibility is
that receptive field sizes of visual interneurons involved in target detection
differ between small and large workers, so that each cell receives input from
seven ommatidia in small workers and from only a single ommatidium in large
workers. This would be reasonable since smaller ommatidia will suffer more
strongly from signal-to-noise problems. Small bees possess ommatidia with
smaller diameters with lower rates of photon capture over time and thus
provide a worse signal-to-noise ratio than do large ommatidia
(Snyder, 1979;
Land, 1981
). The excitation of
only one ommatidium by a small object might not be sufficient for reliable
detection. A summation of signals from several ommatidia at a higher neural
level, as is realised in neural superposition eyes
(Land, 1999
), increases the
signal-to-noise ratio and might also improve reliable detection by small bees.
Conversely, large bees with about 50% larger ommatidial diameter benefit from
a better signal-to-noise ratio and might be able to waive a subsequent neural
summation. Their visuo-spatial resolution might be directly limited by the
ommatidial array.
The other possible interpretation is that the degree of neuronal
convergence is identical in small and large workers and that workers of all
sizes pool the responses from seven ommatidia. In this case, we would have to
assume that a single ommatidium is seven times more sensitive in a large
worker than in a small worker. An increase in lens diameter of about 50% would
result in an increase of aperture of 2.3-fold. But bees with larger eyes
also have longer and wider rhabdoms and thus more membrane surface with a
higher number of visual pigments to increase photon capture
(Kirschfeld, 1976
;
Warrant and McIntyre, 1993
).
Therefore, it is indeed conceivable that larger lenses combined with larger
rhabdoms might cause the 7-fold increase in sensitivity.
Two unambiguous ways to quantify receptive field size would be to use
sinusoidal gratings of varied spatial frequency
(Wehner, 1981;
Srinivasan and Lehrer, 1988
)
or to measure the minimum separable distance between two points. Here, we were
concerned with performance of bees at a biologically realistic task, that of
flower detection. In future experiments, it will be especially interesting to
see if the extent of pooling in a given sized worker is hard-wired or whether
it changes with the intensity of the illumination. There is evidence for this
in movement-detecting neurons of flies
(Dvorak et al., 1980
;
Srinivasan and Dvorak, 1980
)
and in grating resolution in honeybees
(Warrant et al., 1996
).
Behavioural ecologists have long been interested in the importance of eye
design for navigation (Land,
1999; Wehner,
1981
), foraging efficiency
(Dafni and Kevan, 1995
;
Macuda et al., 2001
;
Spaethe et al., 2001
) and mate
search (Rutowski, 2000
;
Vallet and Coles, 1991
). Our
results allow quantitative predictions of how visually constrained
behavioural ability changes with compound eye optics. Data on the optical
system alone are not sufficient to determine single object resolution
capability. Information about subsequent neuronal processing, gained from
behavioural experiments, is indispensable.
Polymorphism of eye optics is not uncommon in arthropods. Many species
exhibit a sexual dimorphism of the eyes: males often have acute zones with
increased facets and reduced interommatidial angles. These zones are used in
rapid pursuit of flying females (Land,
1999; Menzel et al.,
1991
). As an example of polymorphism within a sex, eye optics of
Cataglyphis ant workers are also scaled with body size
(Zollikofer et al., 1995
). But
all of these studies have stopped short of actually measuring the behavioural
performance in target detection and its correlation with eye optics. We show
here that, if eye optics alone are quantified, one might even underestimate
the differences in behavioural ability at target detection that exist between
members of the same species or between different species.
Large bumblebees might be the `acute vision specialists' of the bee colony,
whose workforce might be most efficiently employed in tasks such as searching
for flowers. Indeed, large bees contribute disproportionately to colony
foraging intake: they harvest significantly more nectar per unit foraging time
than do small bees (Spaethe and
Weidenmüller, 2002). Also in line with our prediction, large
bees exhibit a higher propensity to forage rather than to perform household
duties such as brood care and nest cleaning
(Cumber, 1949
). We also
conjecture that large bees might be less constrained by low light intensities
than are small bees and might thus start foraging earlier in the morning and
stop later in the evening. We conclude that our understanding of task
specialization in social insects might greatly benefit from considering
sensory and cognitive differences between individual animals
(Thomson and Chittka, 2001
;
Chittka et al., 2003
).
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Acknowledgments |
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Footnotes |
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