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First published online February 15, 2008
Journal of Experimental Biology 211, 816-823 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.010546
Vision in the nocturnal wandering spider Leucorchestris arenicola (Araneae: Sparassidae)
1 Department of Zoology, University of Zürich, Winterthurerstrasse 190,
CH-8057 Zürich, Switzerland
2 Department of Cell and Organism Biology, University of Lund, Helgonavägen
3, Lund, Sweden
3 Gobabeb Training and Research Centre, PO Box 953, Walvis Bay, Namibia
* Author for correspondence at present address: Forschungsinstitut Senckenberg, Senckenberganlage 25, D-60325 Frankfurt am Main, Germany (e-mail: noergaard.thomas{at}gmail.com)
Accepted 2 January 2008
 |
Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1References |
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525 nm in
the posterior and anteriomedian eyes, and at 540 nm in the anteriolateral
eyes. Theoretical calculations of photon catches showed that the eyes are
likely to employ a combination of spatial and temporal pooling in order to
function at night. Under starlit conditions, the raw spatial and temporal
resolution of the eyes is insufficient for detecting any visual information on
structures in the landscape, and bright stars would be the only objects
visible to the spiders. However, by summation in space and time, the spiders
can rescue enough vision to detect coarse landscape structures. We show that
L. arenicola spiders are likely to be using temporal summation to
navigate at night.
Key words: nocturnal navigation, visual field, electroretinogram, spectral sensitivity, temporal summation, spider navigation
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1References |
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). During daytime the spiders avoid the lethal temperatures
on the desert surface by staying in burrows dug into the sand. The burrows are
silk-lined tunnels that can be occupied for several months
(Henschel, 1990). At night,
hunting and searches for mating opportunities are the main reasons for the
spiders to leave their burrows. Adult females and immature spiders of both
sexes occupy territories of about 3–4 m radial distance around their
burrows and predominantly limit their surface activity to this area. Adult
males, however, will often venture out on long searches for females and mating
opportunities. These searches can take them several tens of metres away from
their burrows (Nørgaard et al.,
2003). Having left the safety of their burrows, the spiders are
then faced with the task of returning to their point of departure (the
burrow). Both sexes and all life stages are capable of doing so via
nearly straight-line trajectories at the end of often circuitous excursions on
the desert surface. In adult males, homeward walks of more than 100 m have
been recorded (Nørgaard,
2005). Even though the 3–4 m homing distances of females and
immature spiders are not as remarkable as the homing distances covered by the
adult males, they are still greater than those found for any previously
studied spider (e.g. Seyfarth et al.,
1982; Görner and Class,
1985; Dacke et al.,
1999; Ortega-Escobar and
Muñoz-Cuevas, 1999). The problems involved in homing over
distances of 3–4 m (adult females and immature spiders) and several tens
of metres (adult males) are essentially the same insofar as neither can be
done by pure ideothetic navigation alone
(Benhamou et al., 1990). Homing
over distances of the order performed by both sexes of L. arenicola
spiders therefore suggests that external cues are used for minimising the
detrimental effect of the inevitable accumulation of errors during
(ideothetic) navigation over long distances
(Benhamou et al., 1990). Prior
studies, mostly done on adult male L. arenicola spiders, have
excluded several external cues as being necessary for the spiders during
homing. The sun, the moon and the polarized light patterns in the sky are not
necessary for the spiders to return to their burrows
(Nørgaard et al.,
2006a). Nor is the direction of gravity, i.e. slope of substrate,
or audible cues, i.e. vibration beacons or olfactory stimuli
(Nørgaard et al., 2003;
Nørgaard et al., 2007;
Nørgaard, 2005). The
diurnal eusocial hymenopterans, e.g. bees and ants, are among the most
impressive and well-studied arthropod navigators, and vision plays a key role
in the strategies they employ to avoid accumulating navigational errors (for
reviews, see Wehner, 1982;
Wehner, 1992;
Wehner and Srinivasan, 2003).
Although L. arenicola spiders are nocturnal and predominantly active
during the moonless times of the night
(Nørgaard et al.,
2006a), a navigational strategy based on vision should not be
excluded straightaway. Insects, with their compound eyes, have been shown to
be able to navigate under very dim light conditions
(Warrant, 2004). Unlike
insects, spiders have single-lens camera-type eyes. The comparatively larger
lens diameter of this eye design should allow for photon catches high enough
to be useful in low light intensity situations
(Nilsson, 1990). Hence, vision
could possibly be used by L. arenicola spiders even at night when the
animals navigate back to their burrows in the dark.
Leucorchestris arenicola is a large spider. Adults can weigh up to
5 g, and their leg span when standing often exceeds 10 cm. Females are
generally slightly heavier than males because of their larger opisthosoma,
while the males have longer legs. Like most spiders, L. arenicola has
eight eyes forming an anterior and posterior row on the carapace, with both
rows being composed of four eyes (Fig.
1A). The eyes of spiders can be classified into four pairs
according to their relative positions on the carapace: the anterior median
eyes (AMEs), the anterior lateral eyes (ALEs), the posterior median eyes
(PMEs) and the posterior lateral eyes (PLEs;
Fig. 1B). The AMEs are referred
to as the principal eyes, whereas the other three pairs are termed secondary
eyes. The AMEs differ from the other eye pairs in morphology and development
(see Blest, 1985). They contain
an everse retina with the light-absorbing parts, the rhabdoms, projecting
towards the lens, and there is no reflecting tapetum behind the retina.
Furthermore, in many spiders the retinae of the AMEs have muscle attachments
to control the direction of vision (Foelix,
1996). In the secondary eyes (ALEs, PMEs and PLEs), the retina is
inverse and lined by a reflecting tapetum; there is no muscular movement of
the retina.
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). In the
present account we explored the possibility that vision is involved in the
impressive homing abilities of L. arenicola, and whether all or only
some of the four pairs of eyes are involved in homing navigation. We also
investigated how the different eyes might be tuned to their visual tasks. |
MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1References |
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The field experiments were carried out on the higher flood plains along the
northern side of the ephemeral Kuiseb River near the Gobabeb Training and
Research Centre in the central Namib Desert (23°33'S;
15°02'E). This area is only flooded by the Kuiseb River in years
with exceptionally high rainfall. It is characterized by open areas
interrupted by Acacia erioloba and Faidherbia albida trees.
This area was chosen because of the large population of L. arenicola
spiders it contained. The spiders were located in the early morning hours by
following their night-time tracks in the sand surface that led to their
burrows. Then the spiders were dug out. Immediately after capture, the eyes of
the spiders were carefully covered with black paint. To ensure that this
treatment did render the eyes opaque, the procedure was tested on the
exoskeletons from moulted spiders, and light transitioning through the lenses
was observed under a microscope. After this procedure, the spiders were
released and induced to build a new burrow at the location at which they had
been caught. This was done simply by placing the spiders under a translucent
cage. Unable to escape and exposed to daylight, the spiders promptly built a
new burrow. In nearly all cases, the spiders remained at the location after
the cage had been removed. Details of the spiders' activities and movements
were monitored by reading the tracks in the sand
(Nørgaard et al.,
2006b). The furthest measurable distance from the burrow and the
number of returns to the burrow made by each spider were recorded. The number
of returns made by each spider in the different groups was used as a measure
of their ability to navigate homeward.
Optics
In the laboratory the spiders were kept on a 12 h:12 h dark:light cycle at
a temperature between 22 and 24°C. The optics of the eyes were studied
ophthalmoscopically (Nilsson and Howard,
1989), exploiting the effect of the reflecting tapetum
(Fig. 2A). The visual fields of
the lateral eyes and the PMEs were measured by means of a goniometer. Since
the AMEs of L. arenicola have no tapetum, the visual fields of these
eyes cannot be obtained in the same way as for the secondary eyes. Instead,
their focal length was measured by employing the hanging drop technique
(Homann, 1928), and the shape
of the retina was determined by histological sectioning. In the focal length
measurements, both AME lenses from three dead adult spiders (two males and one
female) were used. In each of the six eyes the shape of the visual field was
then determined by measuring the angles from the nodal point to the edges of
the retina. Video recordings were used to establish how the spiders carried
their prosomas while walking, so that the measured visual fields could be
plotted onto a sphere, the equator of which coincided with the horizon
skyline. In the secondary eyes the receptors appeared as dark dots against the
bright background of the tapeta. The inter-receptor angle (
) of
these eyes was calculated by measuring the linear distance between the
receptors and comparing this to a scale with a line of points of known angular
separation. F-numbers of the AMEs were calculated by applying the
equation F=f/D, where f is the focal length and
D the lens diameter. The optical geometry and receptor dimensions
were determined from semithin (2.5–3.0 µm) sections of eyes fixed in
aldehyde (glutaraldehyde and paraformaldehyde) and embedded in plastic (see
Nilsson and Ro, 1994).
Horizontal and vertical sections were taken from the eyes of female L.
arenicola spiders (Fig.
2C). The inter-receptor angle () of the AMEs was
calculated using the equation =s/f (radians),
where s is the receptor separation determined using the histological
sections and f is the focal length
(Land, 1997).
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Spectral sensitivity
The spectral sensitivities of the spiders' eyes were determined using
standard methods of electroretinogram (ERG) recordings (e.g.
Barth et al., 1993). The
spiders were fixed in a goniometer, which allowed for precise angular
adjustment of the spiders' eyes under the illuminating ophthalmoscope
(xenon-arc lamp Osram 75W XBO). V–logI curves were
obtained in dark-adapted eyes by using neutral density filters covering a
range of 8 log units in 0.5 log unit intervals. Fourteen interference filters
(Oriel) with half-widths of 20 nm were used in 30 nm steps spanning a spectral
range of 350 nm to 740 nm. Stimuli were 15 ms rectangular flashes separated by
1 min. The ERG recordings were made by placing a glass microelectrode close to
the edge of the corneal lens such that the electrolyte established direct
contact with the eye. A thin, sharply pointed silver wire inserted into a leg
joint membrane formed the reference electrode. The recorded signal was
amplified 1000 times with a DAM 50 amplifier (World Precision Instruments,
Sarasota, FL, USA) using a 1 Hz highpass filter, a 300 Hz lowpass filter and a
50 Hz notch filter (World Precision Instruments). All ERG data were
transferred directly to a computer using a Data Translation 12 bit USB A/D
converter and Scope software version 2.2.0.30 (Data Translation, Marlboro, MA,
USA). The spectral sensitivity curves obtained from the ERGs were compared
with theoretical curves (Govardovskii et
al., 2000). Since the spiders under natural conditions are
nocturnal, the specimens used in the ERG experiment were all dark adapted.
Four adult spiders (one male and three females) were used for the ERGs. The
procedures for each eye type were repeated twice on each spider, giving a
total of eight V–logI and spectral curves for each
type of eye. All spiders survived the treatment.
Temporal summation
While walking, the spiders often interrupt their walking paths and stay
motionless for some time. In order to examine whether or not L.
arenicola employs extended temporal summation as a strategy to allow for
reliable night vision, the duration of these stance phases was recorded and
correlated with the relative ambient light intensity. The rationale for this
experiment was that if the spiders used temporal summation, a negative
correlation between stance duration and ambient light intensity should exist:
the less light available, the longer the stance phases should be. This
question was tested in the field by video recording the spiders as they left
their burrows (Sony DCR-TRV60E digital video camera). As males leave their
burrows more often than female and immature spiders, only males were used in
this experiment (N=12). The video camera can record with infrared
(IR) light, which is invisible to the spiders, as the only light source. The
field of view of the camera covered an area of approximately 2 mx2 m.
This area was illuminated by the IR light source of the camera and in addition
by two IR-LED clusters each containing 15 LEDs (peak wavelength 940 nm). Male
spiders had previously been placed at the location of the recording (method
described above). The video recordings yielded data about both the duration
and the time of occurrence of the stances. As the camera recorded at 30 frames
s–1, the duration of the stances was calculated from the
number of frames during which the spiders did not move. Stance duration was
correlated with the existing relative ambient light intensity measured by
means of a Research Radiometer ILT 1700 and a SHD033 detector (International
Light Technologies, Peabody, MA, USA). The detector was pointed at a white
paper surface at an angle of 45° from a distance of 20 cm. Each
measurement was averaged over 1 min using a 2 Hz sampling frequency. All light
intensity data were normalised to the highest measured value, i.e. setting the
highest measured value to be equal to 100 in order to achieve a measure of
relative ambient light intensity. A video recording of one or more stances at
a specific ambient light intensity was termed a recording event. For technical
reasons the relative ambient light intensity recording had to be made
approximately 150 m from the location of the video recording.
Statistical procedures
The Kolmogorov–Smirnoff test was used to test for Gaussian
distribution of the data and Bartlett's test was used to test for homogeneity
of variances. When two variables were tested, Student's unpaired
t-test was used. When three variables were tested, the data were
analysed by one-way ANOVA followed by the Tukey–Kramer post-hoc
test. In one instance the data did not pass the Bartlett's test and therefore
the non-parametric Kruskal–Wallis test and Dunn's multiple comparisons
post-hoc test were applied.
Likewise, as one of the variables was found not to belong to a Gaussian distribution (data failed the Kolmogorov–Smirnoff test) the non-parametric Spearman rank correlation was used in the test for correlation between relative ambient light intensity and stance duration.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1References |
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In summary, the AMEs and the lateral eyes are both involved in nocturnal navigation. There was a slightly better (though not significantly better) homing performance if the spiders could use their forward-pointing AMEs and ALEs. The PMEs, however, are apparently not used for night-time navigation.
Optics
The video recordings showed that the walking spiders tilted their
opisthosoma at an angle of 10–15° relative to the horizon. Taking
this tilt angle into account, the measured visual fields of the secondary eyes
and the computed visual fields of the primary eyes were plotted onto a sphere
(Fig. 4). The visual fields of
the ALEs and PLEs turned out to be similar in shape, both being horizontally
elongated and, though overlapping slightly, providing the spiders with an
extended view of the surroundings along the horizon. Only to the rear was
there a gap of 40–50° in their combined field of view. The visual
fields of the PMEs covered the remaining upper part of the hemisphere with
little or no overlap with the lateral eyes. Thus, as the animal is always very
close to the ground, the three secondary eye pairs provide the spider with an
almost complete view of its surroundings. The visual fields of the AMEs were
nearly circular and overlapped with each other (at least when both retinae
were pointing forward) and considerably with the ALEs. By observing the
spiders under the microscope it became obvious that the AMEs are provided with
muscles allowing for retina movements. The AME visual fields were plotted onto
the sphere in an approximately forward-looking direction
(Fig. 4). However, movements of
the retina could considerably extend the effective visual fields of the
AMEs.
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=2.5° (see Materials and methods). The absolute sizes
of the lenses varied, of course, with body size but the largest lens diameters
were always found in the AMEs (Table
1). There were no apparent differences in eye positioning or lens
size between male and female L. arenicola.
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The retinae of all pairs of secondary eyes proved to be of the simple type
typical of sparassid spiders (Fig.
2B) (Land, 1985;
Blest, 1985) with
ophthalmoscopically determined values of 2.15±0.03°
(ALEs), 2.10±0.03° (PLEs) and 3.34±0.06° (PMEs;
mean±s.e.m., N=40 for all eye pairs). There was no indication
that the tapetae of the secondary eyes had polarization reflective properties
as is the case in another wandering spider, Drassodes cupreus
Blackwall (Dacke et al., 1999).
The rhabdoms were generally shorter in the secondary eyes than in the AMEs
(Table 1).
ERG recording
All recorded ERGs from the eyes of L. arenicola revealed cornea
negative potential differences similar to ERGs recorded from the nocturnal
ctenid Cupiennius salei Keyserling
(Barth et al., 1993). The
spectral response curves of all eyes showed a single peak indicative of only
one photopigment in the photoreceptors of each eye
(Fig. 5). In the AMEs, PMEs and
PLEs, these measured peaks were located at 500 nm, whereas the measured peak
in the ALEs was at 530 nm. However, theoretical spectral sensitivity curves
(Govardovskii et al., 2000)
showed the best fit for peak values of 541 nm (ALE,
R2=0.920), 525 nm (AME, R2=0.915), 529
nm (PLE, R2=0.922) and 523 nm (PME,
R2=0.901), using the least sum of the square method
(Fig. 5). The eyes of L.
arenicola are thus sensitive in the green area of the spectrum, with the
ALEs having their spectral sensitivity shifted to slightly longer wavelengths
than the others. The minimum temporal half-widths of impulse responses in the
ERGs were roughly 50 ms in all eyes (Table
1).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1References |
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). Although the
homing distances can differ by orders of magnitude, both sexes and all life
stages of L. arenicola must essentially solve the same navigational
task of finding the way back to the safety of the burrow after each
above-ground excursion. In the present account we report results from both
sexes and all life stages of L. arenicola. In none of our experiments
did we observe noteworthy differences between sexes and life stages.
In the majority of nocturnal spiders, vision is believed to play a lesser
role, or no role at all, in mediating behavioural responses
(Foelix, 1996). However, our
findings presented here show that L. arenicola requires vision in its
nocturnal behaviour. It is active even at the darkest times of night
(Nørgaard et al.,
2006a) and yet appears to rely heavily on vision when returning to
its burrow. All eyes except the PMEs were found to be used for this purpose,
and by covering them all we were able to disrupt the spiders' homing abilities
almost completely. On the other hand, the spiders were occasionally found to
be capable of navigating successfully without vision over distances shorter
than 0.5 m. This ability is most likely to be the result of the spiders being
able to rely completely on ideothetic path integration when returning to the
burrow over such short distances. Such non-visual returns from short distances
were never found in adult males with all eyes covered. This is probably due to
the fact that adult males most often walk much further than 0.5 m away from
their burrows. Ideothetic homing over distances exceeding 0.5 m does not
appear to be possible, and finding the burrow entrance by random searches is
highly unlikely, especially for males returning from up to 100 m away.
The optical measurements of the visual fields of the spiders' eyes show that all eight eyes together provide a nearly full view of the spider's visual surroundings (Fig. 4). The horizontally elongated shapes of the visual fields of the lateral eyes provide these eyes with a broad view of the horizon. Hence the lateral eyes might be involved in detecting features of the horizon skyline. The PMEs are apparently dedicated to covering the upper part of the visual hemisphere.
The size of the lenses of the eyes should allow for high photon catches.
They are very probably an adaptation to the dim light conditions prevailing in
the desert at the times of night when the spiders are active
(Nørgaard et al.,
2006a). The raw spatial resolution of the secondary eyes is
sufficient for detecting the few apparent landmarks, e.g. grass hummocks,
present in the spiders' habitat. Stars or star constellations near the horizon
where they can be perceived by the AMEs, ALEs and PLEs could also potentially
be used by the spiders to obtain compass information. In some spiders
(Agelena labyrinthica Clerck and Lycosa tarantula Linnaeus),
the AMEs have been found to detect polarized light, possibly for navigational
purposes (Görner and Class,
1985; Ortega-Escobar and
Muñoz-Cuevas, 1999). However, L. arenicola is
fully capable of navigating home on moonless nights well after astronomical
twilight when skylight polarization has entirely gone
(Nørgaard et al.,
2006a). The poor alignment of the rhabdomeres within the retinae
of the secondary eyes is in accord with the fact that polarization cues are
not available to L. arenicola during the times of night when the
spiders are most active. The PMEs with their coarse spatial resolution and
their dorsally orientated visual fields could be involved in predator
detection.
The spectral sensitivity curves obtained from the ERG recordings indicate
that all eyes are colour-blind. When fitting the data points to a theoretical
opsin curve the results will always improve if the theoretical curve is the
sum of several curves. Using a single opsin curve provided good correlations
(R2=0.90–0.92), though, which is why we conclude
that all the eyes probably contain a single opsin only. The short receptors
would not be expected to generate any broadening of the spectral sensitivities
by self-screening, and the recorded functions should therefore be close to the
spectral absorbance of the photopigments themselves
(Warrant and Nilsson, 1998).
The measured ERG responses of the AMEs, PLEs and PMEs show the best fit to
opsins with peak sensitivity close to 525 nm, while the ALEs have the best fit
to an opsin peaking at about 540 nm. The difference between the measured ERG
values below 410 nm and the expected theoretical values is likely to be an
effect of UV absorption by the lenses. It is interesting to note that the ALEs
appear to have a different photopigment peaking at 540 nm, although the
difference in peak sensitivity is not large. The differences in the spectral
sensitivities between the AMEs and the ALEs and their overlapping visual
fields further strengthen the previous notion that these two pairs of eyes are
involved in different visual tasks. Our results suggesting a single
photoreceptor type in each retina are in contrast with the results from the
eyes of jumping spiders (Blest et al.,
1981), where two receptor types, a UV receptor and a blue
receptor, are generally found. We do not have any data directly explaining
this difference, but having only a single receptor type will in general
increase the overall sensitivity, which may be highly beneficial to L.
arenicola when operating at extremely low light intensities.
Even though all the eyes are of the camera type, and are larger than in
most other spiders, lenses of less than half a millimetre will not catch much
light under starlight conditions when the animals exhibit maximum above-ground
activity (Nørgaard et al.,
2006a). To elaborate on this problem, we used our measured values
of lens diameter, retinal sampling, receptor length and integration time to
calculate the photon catch per receptor and integration time in the different
eyes under starlight luminance (Table
1, Appendix 1). The results show that in all eyes individual
receptors detect roughly one photon per integration time. Because the
statistical uncertainty (standard deviation) of photon arrival is the square
root of the mean, counts of one photon do not provide any usable information
at all. Using the highest possible temporal and spatial resolution allowed by
the eyes, the spiders would therefore be completely blind to landscape
structures in the starlit Namibian desert. Since the behavioural experiments
showed that vision is necessary for successful homing during night excursions,
the spiders must use spatial and/or temporal summation to overcome photon
noise. A workable noise level is obtained only after each image channel has
received an average of 50–100 photons in each count. Realistically, such
summation cannot be achieved by spatial pooling alone, because this would
almost entirely abolish spatial resolution. The same argument holds for using
pure temporal summation, because this would extend the integration time beyond
any known example and would render the animals completely blind even when
walking slowly. Hence, a combination of temporal and spatial pooling would
clearly be the best strategy, because it compromises neither spatial nor
temporal resolution beyond realistic limits
(Warrant, 1999;
Warrant, 2004). If we assume
spatial pools of seven receptors (3x3x3 within a hexagonal array)
and a 10-fold increase of integration time, the pooled visual channels would
cover an acceptance angle of 6–10°, would allow for a shutter speed
of about 0.5 s, and would be able to detect contrast levels as low as
10–20%. This would leave the animals with coarse but functional vision
at starlight intensities.
If the spiders stop and collect visual information at regular intervals
during night-time excursions, they could push the balance between spatial and
temporal pooling towards more acute spatial vision. Indeed, when observing the
spiders at night during their excursions, one immediately notices their habit
of pausing for a while between walking short distances. Less than 2 m seems to
be the usual distance travelled between two pauses
(Nørgaard et al.,
2003). Standing still between short intervals of walking would
enable the spiders to engage in temporal summation and thus avoid too heavy a
loss in spatial resolution. Indeed, when correlating the duration of the
stances that the spiders make during their journeys with the relative ambient
light intensity, it is likely that temporal summation is the method used to
allow them to have night vision. At the lowest light intensities the measured
stance durations approached 1 s. Such extended collection of light would allow
the spiders even better spatial resolution than predicted by our theoretical
calculations, albeit preventing the spiders from seeing moving objects. The
rather high variance in the times the spiders spent stationary
(Fig. 6) could result from the
possibility that the spiders collect not only visual information when standing
still. Leucorchestris arenicola relies heavily on substrate-borne
information during prey capture, and is likely to do so for predator detection
as well. Since detection of substrate vibrations is hindered when walking, the
spiders are probably not only seeing but also `listening' when standing still.
An additional and probably the original reason for pausing is, of course, to
catch breath: respiration in spiders is typically insufficient to sustain
continuous fast locomotion (Foelix,
1996). Recording the pausing behaviour under laboratory conditions
was not possible, and in field experiments many factors, e.g. the presence of
other animals, cannot be controlled. If the spiders are indeed looking for
landmarks, i.e. stationary objects, the loss of temporal resolution would not
be too severe a handicap. Landscape snapshots at regular intervals could
provide the spiders with the information necessary for fixing positions during
their night-time excursions. Bright stars or star constellations could in this
way also function as a compass guide for the spiders. However, this would
imply that the spiders are able to compensate for the movements of the stars
across the sky during excursions. The notion that the spiders rely heavily on
temporal summation is further supported by the fact that they mostly, and when
running always, use only six legs. During motion the front pair is pointing
forward, possibly as mechanical `antennae' making up for the diminished visual
abilities.
Our data on eye design and performance in L. arenicola do not
point towards any obvious division of labour between the different types of
eye. The overlapping visual fields of the AMEs and ALEs, however, could
suggest a division of visual tasks between these two pairs of eyes. The larger
lenses of the AMEs allow for a slightly better resolution and/or contrast
sensitivity than is the case with any of the secondary eyes, but the
difference is marginal. The lack of a tapetum in the AMEs is largely
compensated for by the longer rhabdoms in these eyes. Using the absorption
equation for white light (Warrant and
Nilsson, 1998) and assuming an absorption coefficient of 0.0067
per micrometre, the 82 µm rhabdoms of the AMEs absorb 19% of the incident
light and the 48–63 µm rhabdoms of the secondary eyes (effectively
doubled in length by the tapetum) absorb 22–27% of the incident light.
These small differences in the photon capture efficiency seem only to diminish
the effect of the slightly larger lenses in the AMEs. If any division of
visual tasks between these eyes exists, this could perhaps be found in
temporal resolution properties.
As far as the orientation of the visual fields of the various types of eye are concerned, the AMEs covering the forward field of view would be best suited to avoiding obstacles and guiding the final approach to the entrance of the burrow. The lateral eyes (ALEs and PLEs taken together) cover an almost circumhorizontal field of view and hence would be well suited to taking skyline snapshots. Their poor photon catch will effectively prevent them from acting as self-motion detectors during walking. The PMEs, even though mainly monitoring the sky, are apparently not necessary for night-time navigation. Being the smallest eyes, they are possibly involved only in warning of threats approaching from above, if the spider should be forced to leave its burrow during the day.
In conclusion, the present study has clearly shown that despite the nocturnal lifestyle of L. arenicola, vision must play an important role in the spiders' long-distance night-time navigational performances, but the particular way in which the spiders employ vision during homing remains to be resolved. Extended temporal summation appears likely to be the strategy that allows the spiders to have sufficiently high visual acuity during night-time hours. Hence, at this juncture, ideothetic path integration complemented by the use of visual landmark cues is the spiders' most likely mode of navigation.
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APPENDIX 1 |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1References |
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) with the quantum
efficiency, integration time and ambient luminance (see
Land and Nilsson, 2002;
Warrant and Nilsson, 1998):
 |
the acceptance angle of
the receptor (in radians), k the absorption coefficient of the
rhabdom, l the rhabdom length, q the quantum efficiency,
t the integration time and I the ambient luminance.
The value for k was taken as 0.0067 (see
Warrant and Nilsson, 1998) and
q was taken to be 0.4, based on an assumed transduction efficiency of
0.5 and transmission through the eye's optics of 0.8. The ambient luminance,
Q, was taken for a starlit night: 1012 quanta
m–2 sr–1 s–1 (see
Land and Nilsson, 2002). The
remaining values are given in Table
1. |
Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1References |
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