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J Comp Physiol A (2002) 188: 1–12
DOI 10.1007/s00359-001-0273-7
O R I GI N A L P A P E R
Ronald L. Rutowski Æ Eric J. Warrant
Visual field structure in the Empress Leilia,
Asterocampa leilia (Lepidoptera, Nymphalidae):
dimensions and regional variation in acuity
Accepted: 7 December 2001 / Published online: 7 February 2002
Springer-Verlag 2002
Abstract Male Empress Leilia butterflies (Asterocampa
leilia) use a sit-and-wait tactic to locate mates. To see
how vision might influence male behavior, we studied
the morphology, optics, and receptor physiology of their
eyes and found the following. (1) Each eye’s visual field
is approximately hemispherical with at most a 10
overlap in the fields of the eyes. There are no large sexual
differences in visual field dimensions. (2) In both sexes,
rhabdoms in the frontal and dorsal ommatidia are
longer than those in other eye regions. (3) Interommatidial angles are smallest frontally and around the equator of the eye. Minimum interommatidial angles are 0.9–
1 in males and 1.3–1.4 in females. (4) Acceptance angles of ommatidia closely match interommatidial angles
in the frontal region of the eye. We conclude that vision
in these butterflies is mostly monocular and that males
have more acute vision than females, especially in the
frontal region (large facets, small interommatidial angles, small acceptance angles, long rhabdoms, and a
close match between interommatidial angles and acceptance angles). This study also suggests that perched
males direct their most acute vision where females are
likely to appear but show no eye modifications that
appear clearly related to a mate-locating tactic.
Keywords Asterocampa leilia (Nymphalidae) Æ
Butterfly vision Æ Visual field structure Æ Eye
morphology Æ Acute zone
R.L. Rutowski (&)
Department of Biology, Arizona State University,
Tempe, AZ 85287-1501, USA
E-mail: [email protected]
Fax: +1-480-9652519
E.J. Warrant
Department of Zoology, University of Lund,
Helgonavägen 3, 22362 Lund, Sweden
Introduction
Butterflies use vision in many contexts during their lives
to detect and recognize important features of their environment, including potential oviposition sites, adult
food resources, and mates (for review, see Rutowski
2002). Nonetheless, only recently have detailed studies
of their apposition compound eyes been undertaken to
investigate the proximate mechanisms that determine
the performance of their visual system in different behavioral contexts. These studies have focused primarily
on the mechanisms of color vision (most recently Kelber
1999a, 1999b; Kelber and Pfaff 1999; Kinoshita et al.
1999). Less attention has been devoted to the peripheral
features of eye morphology that determine the acuity of
their vision and thereby their ability to recognize shape
and form and to detect conspecifics and other biologically important objects in their environment. These peripheral features especially include the diameter of the
corneal facet lenses overlying each ommatidium, the
angle between the optical axes of adjacent ommatidia
(the interommatidial angle D/), the acceptance angle of
the photoreceptors (Dq), and the length of the rhabdoms
(Land 1989, 1990, 1997; Warrant and McIntyre 1992,
1993). All influence acuity and, in general, regions of the
eye with high visual acuity – known as ‘‘acute zones’’ –
are characterized by large facet lenses, small D/, Dq that
matches D/, and long rhabdoms (Land 1989, 1997).
In the last few years we have studied the mate
searching behavior of the Empress Leilia butterfly, Asterocampa leilia (Nymphalidae). In this species, males
occupy and defend perching sites where they sit and wait
for females to appear (Austin 1977; Rutowski and Gilchrist 1988; Rutowski et al. 1991). While waiting, they
adopt one of two perching positions: (1) on the ground
with their body axis (and the equator of their visual
system) pitched up at an angle of 20–25, or (2) on
vegetation about 0.85 m off the ground, with the equator of the visual system held horizontally (via head
positioning that compensates for body orientation;
Rutowski 2000a).
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Experimental data indicate that males perched on the
ground are more likely to detect passing conspecifics
than males perched off the ground (Rutowski et al.
2001). This is likely because the two perch locations
present different backgrounds against which conspecifics
must be detected. Vision thus plays an important role in
mate detection, and knowledge of how their eyes are
designed – especially with regards to acuity, the location
of acute zones and the structure of the visual fields – can
greatly help us understand their mating behavior.
Studies of regional variation in facet diameters indicate that the Empress Leilia has frontal and equatorial
zones with enlarged facets, especially in males (about
21 lm in diameter; Ziemba and Rutowski 2000). Enlarged facets often indicate the presence of an acute zone.
Indeed, frontal and equatorial acute zones are probably
quite common in Lepidopteran apposition eyes (Land
1989, 1990), and are even found in the superposition eyes
of the day-active hummingbird hawkmoth (Warrant et al.
1999). In this study we examine these acute zones in more
detail and document regional variation in D/, Dq, and
rhabdom length to see if there is support for the expectation that vision is most acute in the frontal and equatorial regions of the eyes. In addition, we describe visual
field dimensions and the degree of binocular overlap, and
report on sexual differences in ommatidial arrangement
and how these relate to observed sexual differences in eye
size and facet diameter (Rutowski 2000b; Yagi and
Koyama 1963; Ziemba and Rutowski 2000). Finally, we
relate the design of the eyes and the structure of the
visual fields to the reproductive and other behaviors
of these butterflies and other arthropods.
Materials and methods
Animals
We obtained the specimens used in this study either as adults in the
field or reared from eggs collected from females from the field.
Collecting locales were in central Arizona, USA, and have been
previously described (Rutowski et al. 1994).
Visual field dimensions
To measure the size of the visual field, we mounted the isolated
head of a butterfly at the center of curvature of a goniometer. The
goniometer was then placed onto the foot-plate of a macroscope.
The head was placed (neck side down) at the center of the horizontal stage of the goniometer, and secured there with a small
amount of petroleum jelly so that its rear side was parallel to the
plane of the stage. We then adjusted the head’s position so that (1)
the origin of the three goniometer axes was in the center of the
head, and (2) the three goniometer axes were lined up with the
dorsal-ventral (yaw), anterior-posterior (roll), and left-right (pitch)
axes, respectively, of the butterfly’s head. With the stage horizontal,
both eyes then looked vertically upwards into the objective of the
macroscope, and when observed in this position, the eyes were
oriented exactly anteriorly (from the animal’s point of view). The
goniometer allowed us to tilt the stage (and thus the head) in defined angular steps of latitude and longitude, with latitude=0 and
longitude=0 defined as the anterior orientation described above
(‘‘A’’ in Figs. 2–5). Dorsal (‘‘D’’) corresponds to a latitude of+90,
ventral (‘‘V’’) to a latitude of –90, and lateral (‘‘L’’) to a latitude of
0 and a longitude of+90.
To illuminate the eyes we introduced a cover slip, angled at 45,
just beneath the objective of the macroscope. Collimated white
light (from a halogen source) was directed laterally to the cover slip
so that the eyes were illuminated and viewed along the same axis
(‘‘orthodromic illumination’’). This type of illumination reveals the
luminous pseudopupil, or eye shine, that is displayed by many
species of butterflies (Stavenga 1979), including A. leilia. When the
head was properly aligned with the goniometer axes the binocular
luminous pseudopupils moved symmetrically over the surface of
the eyes (relative to their front edges) when the head is rotated
about the pitch axis (i.e., rotated through various latitudes along
the 0 longitude line).
The head was then rotated at 20 increments of latitude around
the dorso-ventral axis and the longitude at which the pseudopupil
in the left eye disappeared at both the front and rear edges of the
eye was recorded. The structure of the goniometer prevented us
from making this observation at latitudes above about 70.
Data were obtained from five males and five females and
plotted on two-dimensional (latitude-longitude) graphs, one for
each sex. A line was then drawn using visual interpolation that
showed the location of the visual field edge. We next cut this graph
into 10 wide strips (along different latitudes) and weighed each and
the part of each that fell within the eye’s visual field. After making
cosine adjustments for area distortions in the two dimensional
projection at increasing latitudes, these weights were then used to
calculate the angular area of the left eye’s visual field contained
within each 10 strip. Finally, by adding these areas together we
calculated the total visual field size for the left eye. Assuming
symmetrical visual fields in the two eyes, we also calculated the
extent of binocular overlap and the size of the region in space
around the head that was not detected by either eye.
Maps of D/
The procedure used to map variation in D/ in the frontal part of
the visual field follows that outlined by Land and Eckert (1985),
but will be briefly reviewed here. The small end was cut from an
Eppendorf vial leaving an opening about 3 mm in diameter. We
then inserted an adult A. leilia with the wings removed into the
large end of the vial until the head just protruded through the small
opening. We then fixed the butterfly in position by gluing the
proboscis to the tube with dental wax. The butterfly was then positioned at the center of a Leitz goniometer and viewed with a
macroscope, as described above. We oriented the head with respect
to the three axes of the goniometer as previously described and then
sprinkled chalk dust lightly on the eye to provide landmarks.
Once the head was properly positioned, we identified a facet at
the anterior edge of the left eye that would be used to define the
origin of the x and y facet rows (x=0, y=0). For hexagonal
packing of ommatidia, the x and y rows are oriented at about 60
to the equator of the eye: the x rows run frontal-ventral and the y
rows frontal-dorsal. The z facet rows run roughly dorso-ventrally.
We then tilted the goniometer through several degrees of longitude
until the pseudopupil was centered on the origin facet. Sometimes
this facet differed by a few degrees of latitude from the zero-latitude
position of the goniometer (due to difficulty in aligning the equator
of the eye with the equator (latitude-zero line) of the goniometer
during placement of the animal). Therefore, it was also sometimes
necessary to tilt the goniometer by a few degrees of latitude in order
to center the pseudopupil over the origin facet. This number of
degrees was later used to adjust the goniometer coordinates to
match the coordinates of the eye. The location of the origin facet in
goniometer coordinates (latitude, longitude) was recorded, and the
pseudopupil was photographed using a CCD camera mounted
onto the macroscope. The image was directly printed using a
Mitsubishi video printer. We then returned the goniometer to 0
latitude and 0 longitude and began taking a series of photographs
of the luminous pseudopupil in the left eye at 10 intervals of latitude and longitude. Due to the structure of the apparatus we could
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not go beyond latitudes of +60 or –60 or a longitude of 70.
Hence, our observations of the appearance and location of the
pseudopupil were restricted to the frontal region of the eye, which
was, in any event, the region of greatest interest.
From each photograph we were able to determine (relative to
the facet origin) the facet coordinates (x, y) of the facet found at the
center of the pseudopupil, using the landmarks as a guide. From
the goniometer coordinates (latitude and longitude adjusted to
match the coordinates of the eye), and the facet coordinates (x, y),
maps were made showing the projection of every fifth facet row in
visual space. Separate maps were made for the x and y facet rows
and these were superimposed to produce a grid of tetragons, each
tetragon having sides five facets long. Each tetragon thus contained
25 facets, irrespective of its angular projection area. Larger areas
therefore have a lower density of ommatidia and a larger average
interommatidial angle. Using established formulae that correct for
latitude distortions in the projection (Land and Eckert 1985), we
calculated the average D/ for each tetragon and the region of space
(in latitude and longitude) that it viewed. These data were plotted
on a sphere representing three-dimensional space around the animal, and isobars were interpolated to connect regions of space
viewed by parts of the eye with the same D/.
We made such D/ maps for two males and three females. Due
to variation in exactly how the equator of the eye was positioned
relative to the equator of the goniometer we did not sample exactly
the same parts of the eye for each individual. Also, the averages for
D/ might have been different had we used information from the
z facet rows but because the eye is close to spherical we would
not expect these to be greatly different.
Electrophysiology
Standard procedures for intracellular electrophysiology in insect
eyes were used. These are fully described elsewhere (Warrant and
McIntyre 1990). Briefly, a butterfly was inserted into a plastic pipette tip whose end had been sliced off to allow the butterfly’s head
to pass through. A small quantity of bee wax was used to secure the
head to the pipette tip. The butterfly was then mounted onto a
small holder and a tiny hole (five to ten facets wide) cut near the
dorsal margin of the left compound eye. The hole was sealed with
petroleum jelly to prevent it drying out. An indifferent electrode of
thin silver wire was inserted into the other eye. A glass microelectrode (borosilicate glass, filled with 2 mol l–1 potassium acetate,
200–300 MW in vivo) was inserted through the hole, and advanced
ventrally into the eye using a Märzhäuser piezo-driven manipulator. Intracellular penetrations of photoreceptors were distinguished
by resting potentials between –40 mV and –50 mV and depolarizing responses to flashes of light. Responses were amplified on a
Biologic microelectrode amplifier, and digitized on-line using a
MacIntosh computer and LabVIEW software. White light from a
xenon arc lamp was directed to the eye though a 100-lm-wide
quartz light guide whose exit aperture subtended 0.27 at the eye
(i.e., point-source illumination). Light intensity was controlled by
quartz neutral-density filters. The end of the light guide was held in
a cardan arm device that allowed the point source to be placed at
any location on an imaginary sphere centered on the butterfly’s eye.
The point source could thus be moved in known angular steps
throughout the visual field of the eye. Each butterfly was placed in
the apparatus in exactly the same orientation in every experiment,
thereby making it possible to place the point source at known
latitudes and longitudes relative to the anterior point of the eye.
When a photoreceptor was penetrated, the point source could be
positioned on the visual axis of the cell (the direction from which
the maximum response is generated) and the latitude and longitude
of the cell’s axis thus determined. In this way we were able to test
the spatial and temporal properties of photoreceptors viewing
different parts of the eye’s receptive field. Our aim was to advance
an electrode along a dorso-ventral line that traversed the eye’s
equator in the frontal visual field, and record from as many photoreceptors as possible along the way. By doing this we could study
the properties of cells in relation to the local interommatidial angle
(which reaches a minimum near the eye’s equator; see below).
Experiments were performed in both the dark-and lightadapted states at a laboratory temperature of 24C. At least partial
light adaptation was achieved by switching on the ceiling lights in
the laboratory. This gave light intensities equivalent to those encountered at early dusk, about 100–1000 times lower than A. leilia
would normally experience in the wild. Light adaptation in apposition eyes usually takes less than 2 min, but in our experiments
animals were light adapted for at least 10 min. Dark adaptation
was at least half an hour, but usually longer.
Following penetration in the dark-adapted state, the visual axis
of the photoreceptor was located. The response of the cell to a series
of 40-ms flashes of increasing light intensity was then measured (the
V-logI curve). The interval between flashes was 10 s. Following this,
an intensity was chosen that gave a response about 60% of maximum. The point source was then displaced from the cell’s axis and
swept across the receptive field in angular steps of 0.25. At each step
a flash was delivered and the response recorded. These responses were
converted to equivalent intensities through the V-logI curve and
sensitivity values at each angular step calculated. The resulting
‘‘angular-sensitivity function’’ (sensitivity as a function of angular
position) is the photoreceptor’s spatial receptive field and the halfwidth of the function is the acceptance angle Dq, an excellent measure
of spatial resolution: the larger the acceptance angle, the poorer the
resolution (Warrant and McIntyre 1993). Following these measurements, the point source was re-positioned on the axis of the cell,
and the flash length reduced to 2 ms. An intensity was chosen that
elicited a response from the cell no greater than 3 mV in amplitude.
The response of the cell to this impulse of light – the ‘‘impulse response’’ – was recorded 100 times and averaged. The time-course of
this response, notably its time-to-peak, sp, and its half-width, Dt, are
excellent measures of temporal resolution: shorter times indicate
greater resolution (Howard 1981). Impulse responses were fitted to a
log-normal function V(t), that varies with time t. This function depends on only two parameters: sp and a width factor r (Howard
1981):
h
i
2
ð1Þ
V ðtÞ ¼ exp lnðt=sp Þ =2r2
where r is given by ln(sp/s1), with s1 the time taken for the impulse
response to reach 61% of its maximum value. Finally, the power
spectra of impulse responses, and their log-normal fits, were calculated in order to assess the range of temporal frequencies (in Hertz)
that photoreceptors can process. The power spectrum was used to
determine the corner frequency, fc, at which power falls to half
maximum. The corner frequency is a useful measure of temporal
resolving power that can be compared with values obtained from
photoreceptors in other animals.
When possible, the spectral sensitivity of each penetrated photoreceptor was also coarsely measured using a series of interference
filters from 300 nm to 700 nm in 50-nm steps. These filters had a
bandwidth of 40 nm, and were therefore not suitable for accurate
measurements of spectral sensitivity, but were adequate for rough
determinations of photoreceptor spectral class. All experiments
were then repeated in the light-adapted state.
Histology
Standard methods were used for light microscopy. Whole eyes were
placed for 2 h at 4C in standard fixative (2.5% glutaraldehyde and
3% paraformaldehyde in 150 mmol l–1 Na-cacodylate buffer;
pH 7.2). Following this, eyes were rinsed in buffer, dehydrated in
an alcohol series, and embedded in Araldite. Thin (3.5 lm) sections
for light microscopy were stained with toluidine blue.
Results
The structure of the compound eyes
The compound eyes of A. leilia are of the apposition
type (Fig. 1). Presumably, as in other butterflies except
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skippers, they are afocal apposition eyes, with the
proximal tips of the crystalline cones possessing a small
graded-index lens cylinder for improved visual performance (Nilsson et al. 1984; van Hateren and Nilsson
1987). The eyes of males and females appear very similar
in the two section planes we have chosen (Fig. 1): (1)
a horizontal (posterior-anterior) plane through the
equator of the eye (latitude 0), and (2) a vertical (dorsalventral) plane through the lateral point of the eye
(longitude +90). The eyes are not uniform in structure
in either sex. The thickness of the retina, and thus the
length of the rhabdoms, is greatest in the anterior and
dorsal parts of the eye. In apposition eyes regions of the
eye where the rhabdoms are longest are typically regions
with improved visual performance, having greater sensitivity, or higher resolution, or both. As we show below,
the longer rhabdoms of the anterior eyes are indeed
associated with such a region.
The only difference between the sexes may lie in the
dorsal eye. There rhabdoms appear to be somewhat
longer in males than in females (420 lm compared to
320 lm). The rhabdoms in the ventral, lateral, anterior
and posterior parts of the eyes in both sexes have lengths
of around 205 lm, 270 lm, 395 lm, and 295 lm, respectively.
immediately behind the head is not seen by either eye.
The sexes did not appear to be different with respect
to the total visual field size or the degree of binocular
overlap. Males may have a slightly smaller blind spot
at the back of the head.
Visual field size
Fig. 2a–d The visual field of male A. leilia. Data is plotted onto a
sphere that represents the three-dimensional space around the
animal. Lines of latitude and longitude are shown in intervals of
10. a Dorso-posterior perspective. b Dorso-frontal perspective.
c Ventro-posterior perspective. d Ventro-frontal perspective. The
white area is that part of the space around the butterfly that is not
detected by either eye. The light shading is the region of monocular
vision, while the darker shading is where vision is binocular.
Abbreviations: D=dorsal, V=ventral, L=left, R=right, A=
anterior, P=posterior
The visual field of one eye in A. leilia is approximately
hemispherical and overlaps little with the visual field
of the other eye (Figs. 2, 3, Table 1). At the equator
of the visual field, binocular overlap is about 10 and
rises to a maximum of about 20 at the dorsal and
ventral poles of the visual field. Only a small region
Fig. 1 Light microscopic
sections through the eyes of
A. leilia. The two panels at left
show sections in a horizontal
(posterior-anterior) plane at the
equator of the eye (latitude=0). Sections are from a
female (upper) and a male
(lower), where A=anterior,
L=lateral and P=posterior.
The two panels at right show
sections in a vertical (dorsalventral) plane at the lateral
point of the eye (longitude=
+90). Sections are from a
female (left) and a male (right),
where D=dorsal and V=ventral. Scale bar for all parts:
200 lm
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region but here they were generally between 1.3 and
1.4. This indicates that both sexes possess frontal acute
zones, but that in males the acute zone is larger and
sharper.
In both males and females the isobars are stretched
out along the equator which means that D/ changes
more quickly as one goes dorsally or ventrally from the
equator than it does as one goes posteriorly along the
equator. Also, both males show a large region of relatively uniform D/ (1.4–1.7) in the dorsal-frontal region
between latitudes 15 and 45 and extending from the
front around the side of the head to about longitude 40
or 50. This feature is also present in female eyes, but is
less pronounced. Towards the dorsal and ventral poles,
as well as posteriorly, D/ climbs to values over 2 in
both sexes.
Spatial and temporal resolution of the photoreceptors
Fig. 3 The visual field of female A. leilia. All other details as in
Fig. 2
Table 1 Dimensions of visual field characteristics for A. leilia. All
measurements are in units of p steradians. See text for details
Visual field size
Male
Female
One eye (range)
Both eyes
2.21 (2.08–2.37)
2.18 (2.06–2.29)
3.93
3.88
Binocular
overlap
Blind
spot
0.49
0.49
0.07
0.12
Regional variation in D/
Maps of interommatidial angle (D/) for two males
(Fig. 4) and three females (Fig. 5) display several important features of visual field structure in these butterflies. In males, the smallest values of D/ are in the
frontal region of the eye and are between 0.9 and 1. In
females, the smallest D/’s are also found in the frontal
Fig. 4a,b Maps of the interommatidial angle D/ for the left
eyes of two A. leilia males. a
Male 1, with a 22 mm fore wing
length. b Male 2, with a 23 mm
fore wing length. All other
details as in Fig. 2
Intracellular electrophysiological recordings were made
from photoreceptors viewing different regions of the
visual field to measure their spatial and temporal resolution in the light-and dark-adapted states. The cells
we encountered were typically green-sensitive with
peak sensitivity around 530–550 nm. We also recorded
from a single violet cell (peak sensitivity 400–430 nm)
whose visual axis was located near the anterior equator (2 latitude, 10 longitude). This region of the
visual field was also rich in green cells. Ultraviolet
cells, probably common in the retina, were never
encountered.
The spatial receptive fields of the photoreceptors (or
angular-sensitivity functions) are quite narrow and
approximately Gaussian in shape. In Fig. 6 the receptive field of an equatorial cell in a male is shown in the
light- and dark-adapted states. Light adaptation shifted
the V-logI curve 0.8 log units towards brighter intensities, and narrowed the receptive field marginally. In
the dark-adapted state, Dq, defined as the angular
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Fig. 5a–c Maps of the interommatidial angle D/ for the left
eyes of three A. leilia females.
a Female 1, with a 27–28 mm
fore wing length. b Female 2,
with a 24 mm fore wing length.
c Female 3, with a 23.8 mm fore
wing length. All other details as
in Fig. 2
half-width of the angular-sensitivity function (see
Fig. 6), is 1.45, narrowing to 1.23 when light adapted.
In butterfly eyes, as in many apposition eyes, light
adaptation induces an inward migration of lightabsorbing pigment granules within the retinula cells
that removes the wider higher-order waveguide modes
(Land and Osorio 1990). Had our adapting light been
brighter, the angular-sensitivity function may have
narrowed more. A small Dq indicates a narrow receptive field and better spatial resolution (Warrant and
McIntyre 1993).
In several male specimens, and in one female specimen, we were able to traverse a large part of the frontal
visual field from dorsal to ventral, recording from photoreceptors with visual axes located at several different
latitudes. We already know that in the same part of
the eye, D/ varies with latitude, narrowing towards the
equator to form a frontal acute zone (Figs. 4, 5). The
size of Dq also varies with latitude (Figs. 7, 8). In males
Dq is greater at higher latitudes but becomes narrower
towards the equator and broadens again at negative
latitudes. The light-adapted Dq values of four frontal
cells (longitude 10–20) from the eye of a male butterfly
are shown in Fig. 7. A cell whose visual axis was at
latitude +32 in the frontal visual field had Dq=2.19
(Fig. 7a). A cell whose axis was at latitude +15 had
Dq=1.58 (Fig. 7b). Dq reaches its minimum near the
equator: a cell at latitude +1 had Dq=1.37 (Fig. 7c).
At latitude –22 a cell was penetrated with Dq=2.04
(Fig. 7d). Results based on 29 angular-sensitivity functions from 11 cells in a further three light-adapted males
show a similar result (Fig. 8, open circles). All cells
penetrated had their visual axes centered frontally at
longitude +15±4. Those cells with their axes closest to
the equator had the narrowest angular-sensitivity functions (Dq=1.26±0.08). Cells above and below the
equator had greater Dqs. The results obtained from a
single female followed a similar pattern (Fig. 8, filled
circles), although values of Dq were found to be about
half a degree larger than in males.
In Fig. 8, values of D/ taken from Figs. 4 and 5 are
plotted against the Dq observed at the same latitudes. In
males Dq and D/ are comparable at and slightly above
the equator, but away from this region (both dorsally
and ventrally) Dq exceeds D/. At a latitude of around
+35 the ratio (Dq:D/) becomes 1.3. At latitude –22 the
ratio is similar. Near the equator the receptive fields of
neighboring photoreceptors overlap at half-height. The
implications of these results for visual sampling will be
discussed later. Within the limited latitude range investigated in the single female, Dq always exceeds D/, with
Dq:D/ lying in the range 1.3–1.6.
7
insects (Howard et al. 1984), the transition from dark
adaptation to light adaptation mainly affects sp: the
width factor r (Eq. 1) changes only slightly from 0.24 to
0.25. The power spectra of impulses and their log-normal fits show that the faster time courses of light
adapted impulse responses translate into a wider range
of perceivable temporal frequencies compared to the
range in the dark adapted state (Fig. 9b). Corner frequencies, fc, derived from the experimental data, are
8.1 Hz in the dark-adapted state and 28.4 Hz in the
light-adapted state. Had the adapting illumination been
brighter or the temperature higher (as could be expected
in the bright desert habitat of A. leilia), then fc would
almost certainly have been higher, and vision thereby
faster.
Discussion
Visual field size and binocular overlap in A. leilia
Fig. 6 The V-logI curves (a) and angular-sensitivity functions (b)
of a frontal equatorial cell in an A. leilia male in the light- (LA) and
dark (DA)-adapted states. Light adaptation shifts the V-logI curve
towards brighter intensities, and narrows the receptive field. The
acceptance angle Dq is defined as the angular half-width of the
angular-sensitivity function. The curves fitting the data in b are
Gaussians
Unlike their spatial properties, we found little variation in the temporal properties of the photoreceptors at
different latitudes (Table 2). In all cells, the responses to
brief dim impulses of light showed a time-course that
was quite fast in the light-adapted state but slower in the
dark-adapted state (Fig. 9a). A slower ‘‘impulse response’’ in the dark-adapted state is typical for photoreceptors (e.g., Howard et al. 1984). Two characteristic
parameters of the impulse response can be defined: its
time-to-peak, sp, and its half-width, Dt, sometimes used
as the photoreceptor’s integration time (see Fig. 9a).
Both are excellent measures of temporal resolution:
shorter times indicate greater resolution (Howard 1981).
For A. leilia photoreceptors in the dark-adapted state
at 24C, sp=27 ms and Dt=18 ms (obtained from
one cell only). In the light-adapted state at 24C,
sp=16.8±1.2 ms and Dt=10.8±1.5 ms (n=6 cells). If
our adapting light had been brighter the time-course of
the impulse response may have been even faster. The
impulse responses shown in Fig. 9a have also been fitted
with the log-normal function (dotted lines). The model
functions fit the experimental curves reasonably well,
although the model is somewhat narrower on the trailing
side of the impulse response. The light-adapted impulse
response chosen for this figure also shows a slight
overshoot not present in the model. As in many other
As in many insects, the visual field of A. leilia is huge. All
but a small region of space at the back of the head is
examined by at least one eye (Figs. 2, 3, Table 1). There
is little binocular overlap, so vision in A. leilia is largely
monocular. This along with the very small distance between the eyes means that they probably do not rely on
binocular distance estimation in the highly modulated
and controlled flight they display as they move around
the environment. However, when alighting on small
leaves and branches as males do when they perch to
search for mates, and as females do to oviposit, binocular vision may play a more important role. In these
instances, we expect a butterfly will maneuver so that the
object is within the binocular part of the visual field, that
is, along the frontal midline of the body.
Frantsevich and Pichka (1977) proposed that the size
of the visual field and the extent of binocular overlap
found in the eyes of an insect will be adaptively related
to their life style. For example, a life style that involves
detecting small fast-moving objects (mates and prey)
that might appear anywhere in the visual field, such as
found in dragonflies, male hoverflies and drone bees, will
favor eyes with large visual field and consequently little
binocular overlap. Such insects might then rely more on
neural circuits that act as matched filters for targets of
correct size, speed and contrast (Olberg 1981, 1986;
Strausfeld 1991; Gilbert and Strausfeld 1991; Gronenberg and Strausfeld 1991; Vallet and Coles 1993), rather
than on binocular estimations of the size and distance of
objects. At the other extreme are insects that capture
prey with rapid and precisely targeted attacks with
grasping appendages or mouthparts, such as praying
mantises, tiger and carabid beetles, and larval dragonflies. These foraging techniques require precise information on the size and distance to a targeted prey and so
should favor extensive frontal binocular overlap. A. leilia
falls closest to first group. However, because the sexes
are so similar in visual field size and the degree of
8
Fig. 7a–d Angular-sensitivity
functions at four different
frontal locations in the visual
field of an A. leilia male in the
light-adapted state. a latitude
+32, longitude +18. b latitude +15, longitude +10.
c latitude +1, longitude +11.
d latitude –22, longitude +20.
Acceptance angles (Dq) are also
indicated. The curves fitting the
data are Gaussians
binocular overlap, these features seem likely to have
evolved in the context of a problem common to both
sexes, such as predator detection.
Regional variation in spatial acuity
The apposition eyes of A. leilia are similar in design and
visual physiology to those found in other diurnal flying
insects, with frontal and, to a lesser extent, equatorial
zones of relatively acute vision, as indicated by large
facets (Ziemba and Rutowski 2000), long rhabdoms,
and small D/ and Dq (Warrant and McIntyre 1993). The
region of highest acuity is that directed frontally in both
sexes, but females overall have less acute vision than
males. Minimum D/ in the frontal region falls to just
1.3 or 1.4 in females, whereas in males it falls to 0.9.
Similarly, males have larger facets than females. Even
though these differences indicate a sexual difference in
eye design, the dimorphism is not as dramatic as that
found in some other insects (Land 1997; Brännstrom
and Nilsson 2002).
Both sexes display an elongated region of smaller D/
and higher acuity along the horizontal equator of the
eye. A widely accepted explanation for these equatorial
acute zones (or visual streaks) is that for animals such as
fiddler crabs that live in very flat environments these
streaks maximize information gathered in the horizontal
plane where conspecifics and other important visual cues
are most likely to occur (see Warrant 2001 for a review).
A. leilia typically flies and often perches about 1 m off
the ground (Rutowski 2000a), which means that although their environment has a good deal of vertical
relief, with much of the vegetation along their flight
paths being several meters high, their visual streaks
might be especially important for detecting and recognizing conspecifics in the horizontal plane around the
eye.
There are two, not mutually exclusive, explanations
for the decline in D/ and Dq as one goes from the front
to the back of the eye. One suggests that, at least for
males, frontal acute zones, sometimes called ‘‘love
spots,’’ are used to track females whilst in rapid aerial
pursuits that lead to mating (Collett and Land 1975).
The other explanation is that the smooth decline in
D/ from front to back is adaptive in the context of
forward flight through a textured environment (Land
1989). The argument is that when an insect (or any
animal) moves forward, objects it passes move from
front to back in the visual field which creates a
so-called ‘‘flow field’’ of moving features (Gibson 1950;
Wehner 1981; Buchner 1984). As the position of an
object relative to the insect changes during flight there
will be dramatic changes in the angular velocity with
which it moves through the visual field. Objects at great
distance and directly ahead will have a very low
9
Fig. 8 The covariance of interommatidial angle D/ (squares) and
acceptance angle Dq (circles) as one travels vertically through the
visual field of three light-adapted A. leilia males (open symbols) at
around longitude +15, from dorsal positive latitudes to ventral
negative latitudes. Similar data is also shown for a single lightadapted female at around longitude +10 (filled symbols). The
dashed line marks the equator of the eye (latitude 0). Values of D/
are taken from Figs. 4 and 5, and Dq values are based on 29
angular-sensitivity functions from 11 cells (males) and 14 angularsensitivity functions from 6 cells (female). All male cells penetrated
had their visual axes centered frontally at longitude +15±4, while
in females they were centred at 10±4 (horizontal error bars). The
vertical error bars represent standard deviations on the mean Dq
values
Table 2 Temporal properties of photoreceptors in different parts
of the A. leilia eye. Photoreceptors, which were broadly sensitive to
green light, were light adapted. Dt and sp , respectively, the halfwidth and time-to-peak of the temporal impulse response (see text
for details)
Cell
Latitude
Longitude
Dt (ms)
sp (ms)
1
2
3
4
5
16
15
11
–20
–24
5
10
10
19
22
12
11
9
10
10
16
16
16
17
17
angular velocity as the insect moves toward them.
However, as the animal passes the object, its angular
velocity will increase to a maximum when the object
reaches a point 90 from directly in front of the insect,
after which angular velocity (v) will again decrease. If
the photoreceptors throughout the eye have a fixed
integration time Dt (which is not necessarily the case;
Burton et al. 2001), the high angular velocity of objects
at the side will be more likely to cause their appearance
to the animal to blur or smear, or in other words, to
increase in apparent size. This change in angular size
Fig. 9a,b The temporal properties of a photoreceptor (latitude
)20, longitude +19) from an A. leilia male in the light- (LA) and
dark (DA)-adapted states at 24C. a Impulse responses (solid lines)
and their log-normal model fits (dotted lines ), with the definition of
time-to-peak tp, and integration time Dt (inset). For this cell,
tp=26.8 ms and Dt=17.7 ms in the DA state and tp=16.8 ms and
Dt=9.8 ms in the LA state. These values of tp are used for the lognormal fits (Eq. 1), with r=0.24 (DA) and 0.25 (LA). b The power
spectra of the impulse responses (solid lines) and log-normal fits
(dotted lines) shown in a. The corner frequency fc is the frequency at
which the power falls to half maximum (normalized power=0.5).
In this cell fc=8.1 Hz (DA) and 28.4 Hz (LA)
will be approximately vDt degrees. This effectively
widens the p
local optical acceptance angle (Dq) to a new
value of
ðDq2 þ ðvDtÞ2 ) (Srinivasan and Bernard
1975; Snyder 1977). An optimal match between Dq and
D/ is expected to be found throughout the eye to avoid
oversampling (high Dq/D/ ) or undersampling (low Dq/
D/ ) the visual field. Hence, to maintain an optimum
ratio of Dq/D/ (Snyder 1977, 1979) this motioninduced increase in Dq going from the front to the side
should be matched by an increase in D/, as indeed
seems to be the case: D/ increases smoothly from 0.9
10
frontally to 2.0 laterally in males, and from 1.3 to
2.2 in females (Figs. 4, 5).
These arguments suggest that as one goes from the
side to the back of the eye D/ should again decrease.
Our results do not extend to this region of the eye but
we doubt this happens based on small facet diameters
in that part of the eye in A. leilia, observations made
on other insects (e.g., Petrowitz et al. 2000), and our
impression that there would be little benefit of having
high quality vision in that part of the visual field.
Measurements of D/ and Dq from different parts of the
eye have also been made in another butterfly species,
Heteronympha merope (Land 1989). This woodland species is also a nymphalid, but compared to our data from
A. leilia males, it has a somewhat different relationship
between D/ and Dq . Using optical measurements of the
deep pseudopupil, Land (1989 and pers. comm.) found
that in H. merope female Dq was approximately 1.9 in all
parts of the eye, even though D/ varied in ways similar to
A. leilia. This implies that in the frontal eye of H. merope,
where D/ is small, there is significant oversampling,
whereas in the dorsal and ventral parts of the eye there is
slight undersampling. In A. leilia males, we found an
opposite trend: frontally DqD/, which indicates slight
undersampling, but dorsally and ventrally Dq>D/,
indicating slight oversampling. However, in the single
female we managed to examine (Fig. 8, filled symbols) the
situation may be more like that in H. merope: in the
frontal eye Dq is significantly greater than D/. Even
though caution is important when interpreting data from
a single animal, it nevertheless raises the possibility that
there could be a sex difference. Another difference is that
his data were obtained in the dark-adapted state when Dq
is expected to be wider. Our data were obtained in lightadapted conditions; this may explain the oversampling
seen in H. merope’s frontal eye, but not the undersampling found elsewhere.
As mentioned above, improved spatial resolution in
the frontal visual field may also be used in the context of
mate detection. In many insects, notably flies, the males
have well-developed frontal acute zones – or ‘‘love
spots’’ – for detecting and tracking females. A similar
strategy is also found in A. leilia: males leave their
perches to pursue females that they have detected, and
the elaboration of the male’s frontal acute zone, relative
to that of the female’s, has probably evolved in response
to sexual selection in this context. Recent findings in flies
suggest that love spots in males are regions of not only
improved spatial resolution but also improved temporal
resolution (Hornstein et al. 2000; Burton et al. 2001).
Love spot photoreceptors are up to 60% faster than
their counterparts in females (Hornstein et al. 2000) and
20% faster than photoreceptors in other parts of the
male’s eye (Burton et al. 2001). In blowflies, the photoreceptors that view the lateral visual field, where the
optic flow is fastest, tend to be the slowest, which suggests that the temporal properties of the photoreceptors
are not matched to local optic flow as one might predict
(Burton et al. 2001). Rather, in the eyes of male flies it
appears more likely that the spatial and temporal
resolutions of photoreceptors are enhanced frontally to
optimize the tracking of small fast-moving targets, like
females, seen against a natural scene background. In
A. leilia, the improved spatial resolution in males compared to females in the frontal eye (with regards to both
D/ and Dq) is in good agreement with this idea. Whether
temporal resolution is also improved remains to be seen.
Temporal acuity
Our results suggest that the speed or temporal acuity of
vision in A. leilia is quite comparable to that found in
many other insects. With a light-adapted impulse
response that peaks at 16.8 ms (Fig. 9), the eyes of
A. leilia are about as fast as those of other able fliers
(Howard et al. 1984). They are faster than locusts
(sp=21.9 ms) and crickets (sp=22.1 ms), as fast as
drone-flies (sp=16.5 ms) and dragonflies (sp=17.5 ms),
but nowhere near as fast as houseflies (sp=12.0 ms) and
blowflies (sp=7.6 ms; Tatler et al. 2000). The fact that
we found no variation in temporal properties at different
latitudes in the frontal region of the eye does not rule out
the possibility that they vary at different longitudes
along the equator. A recent study in male blowflies has
shown that photoreceptor responses are 20% faster in
the frontal visual field than in the lateral and posterior
visual fields (Burton et al. 2001). As we mentioned
earlier, these faster responses have been interpreted as an
adaptation to improve the detection and tracking of
small moving targets in the frontal visual field, something that would benefit male flies when chasing females.
Whether A. leilia males have this same adaptation
remains to be seen.
The fact that Asterocampa lives in warmer and
brighter conditions than we could supply experimentally
may mean that these butterflies have even faster vision
than we measured. We can account for the difference in
temperature by extrapolating from data given in Tatler
et al. (2000), which show that for blowflies the temporal
corner frequency fc increases by about 5 Hz for every 1
rise in temperature. Males of A. leilia maintain a body
temperature of 38–40C while engaged in mate location
(Rutowski et al. 1994; i.e., at least 14C warmer than our
lab), in which case fc28+(14·5)=98 Hz, which is four
times higher than we measured. A. leilia males may
maintain high body temperatures to exploit fast vision in
the detection and recognition of fast-flying females.
Male vision and mate locating strategies in A. leilia
The observations reported here on the vision of A. leilia
males have implications for understanding their matelocating tactics, especially the causes and consequences
of their perch location and body posture preferences.
Males occupy and defend perches on or adjacent to the
larval food plant, desert hackberry (Celtis pallida),
11
where they sit and wait for females to pass by. As reported in another paper (Rutowski et al. 2001), the
values of D/ and Dq in the frontal region suggest that
the maximum distance at which a conspecific can be
detected will be 3–5 m, an inference which behavioral
experiments generally bear out. However, as the temperature of the air and substrate rise during the morning, males switch from preferring perches on the ground
to perches 0.85 m off the ground on vegetation, most
often on the larval food plant. This change in perch
preference is a classic case of behavioral thermoregulation (Rutowski et al. 1994). But what are the consequences of this change in perch location for successfully
detecting females? Again, behavioral experiments suggest that males perched on the ground are more likely to
detect conspecifics passing through their perching area
than males perched off the ground (Rutowski et al.
2001). The reasons for this are not yet completely clear.
We suspect that the background against which the
conspecifics are viewed is a key issue (Switzer and Eason
2000; Rutowski et al. 2001), but the results reported here
clearly provide no strong evidence of regional variation
in acuity that would explain this result.
When perched above the ground, males orient facing
out into open areas adjacent to the perch and position
their eyes so that the frontal acute zone of the eye, and
the equatorial visual streak, are in the same plane as the
likely flight paths of passing conspecific females (Rutowski 2000a). Interestingly, males carefully position
their head so that the equatorial acute zone remains
close to horizontal regardless of variation in body pitch
and roll (Rutowski 2000a). Given what we have reported
here about the visual system of these butterflies and
what is known of the behavior of females, these perch
preferences and postural adjustments would seem to
maximize the probability that a male would detect
passing females.
In contrast, a male perched on the ground typically
pitches its body upwards 20–30 and there is no evidence
of a broad, dorsally-directed region of high visual acuity
(like that found in some dragonflies (Labhart and Nilsson 1995) that might explain why males on the ground
respond so readily to females passing overhead. But
given that females are so consistent in flying about 1–
2 m over the substrate, a large dorsal acute zone may
have been of no special advantage. When viewed from
the ground, the center of the male’s frontal acute zone
will intersect the plane of typical female flight paths at a
distance of about 1.8 m. At this distance, a female with
her 3-cm wingspan will subtend about 1 at the eye, and
will be easily detected, since acute zone acceptance angles are in the same order of magnitude (Fig. 8). In insects that rely on seeing small dark objects moving
against the sky, pursuit behavior can be initiated even
for objects that subtend a small fraction of the acceptance angle (as in drone bees; Vallet and Coles 1993).
Although D/ and Dq gradually increase, and acuity
decreases, as one travels dorsally from the frontal region
of the eye, the consistent flight height means females
passing directly overhead are actually even closer to the
male and may be detectable even without D/ and Dq as
small as those found in the frontal acute zone.
These arguments suggest why A. leilia males, and
those of other perching butterflies, might show no special
features that appear to be adaptations to their mate-locating tactic among the morphological and optical
measures reported here and elsewhere (Rutowski 2000b).
In fact, although the higher acuity of male eyes is likely a
product of sexual selection in their visually guided mating behavior, the major features of their visual system’s
performance appear to have evolved in other contexts,
especially with respect to overall illuminance levels, demands of flight, and detection of predators that might
attack from any direction . However, there are two additional points to be made. First, there may be features of
the physiology of receptor cells or of the underlying visual networks that enhance the ability of perched males
to detect females and intruding males and so may have
been shaped by sexual selection (as we discussed earlier
for flies). Second, the extreme modification of the dorsal
eye seen in some insects may have been especially valuable when the distance at which prey or potential mates
generally appear or pass is less predictable than in A. leilia
(e.g., dragonflies; Switzer and Eason 2000).
Acknowledgements We thank Lee McCoy, Mark Rivera, Jenny
Drnevich, Randi Papke, Aaron Fritts, Brenda Rascon, and especially Megan Kimball, for their help with various phases of this
project both in the lab and field. We are also grateful to the Department of Biology at Arizona State University and the Department of Zoology at the University of Lund for logistic and other
support, and NSF Grant BNS to R.L. Rutowski for financial
support. The authors are very grateful to Rita Wallén (Lund) for
her expert histological assistance. E.J. Warrant is extremely
grateful for the ongoing support of the Swedish Natural Sciences
Research Council.
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