Visual navigation in desert ants Cataglyphis fortis: are snapshots coupled to a celestial system of reference?
Department of Zoology, Zürich University, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
* Author for correspondence and present address: Department of Animal Ecology, Lund University, Ecology Building, SE-223 62 Lund, Sweden (e-mail: Susanne.Akesson{at}zooekol.lu.se )
Please send reprint requests to
rwehner{at}zool.unizh.ch
Accepted 23 April 2002
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Summary |
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Key words: navigation, visual navigation, landmark guidance, celestial reference system, learning, insect, ant, Cataglyphis fortis
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Introduction |
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If available, landmarks provide the most obvious navigational cue used in the close vicinity of the nest. To investigate whether stored landmark views are spatially oriented within a celestial system of reference, we studied the searching behaviour of desert ants in relation to landmarks arranged around the nest (goal). The goal was located asymmetrically within a square array of four cylindrical landmarks so that there were four localities at which a stored snapshot could be matched with the current retinal images. However, it was only at one of these positions that the snapshot and the current retinal image were in register with the celestial system of reference. In these experiments, we used ants that had returned from a foraging visit to a feeder located at a distant and fixed compass direction relative to the nest. The ants were released from four compass directions: from the training direction (0 °) and from three others of ±90 ° and 180 ° from the training direction. In the latter three cases, the closest hypothetical nest positions given by the landmarks were in conflict with the directional information given by celestial information. Hence, the experiments are designed to provide information about the extent to which a memorized visual snapshot scene can be coupled or decoupled from a celestial system of reference.
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Materials and methods |
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Observations at the feeder started prior to the time when the first ant appeared outside the nest entrance in the morning (between 08.00 and 08.30 h; Coordinated Universal Time+1 h) and continued until at least 16.00 h in the afternoon, when foraging activity decreased.
Experimental arrangement and procedure
We arranged a four-cylinder landmark square around the nest entrance such
that the nest entrance was located asymmetrically relative to the centre of
the landmark square (Fig. 1A).
The landmarks used in the experiments were plastic cylinders, covered with
black paper, of height 40.5 cm and diameter 22.5 cm. The side length of the
landmark square was 282 cm (as measured from the centre of the landmarks).
Correspondingly, the diagonal distance was 400 cm. Two of the sides of the
landmark square were arranged parallel to the geographic northsouth
axis. The nest entrance was located inside the landmark square along a
diagonal line 100 cm northwest from the landmark located in the southeast
corner of the landmark square (Fig.
1A).
During the first 2 days of training, we captured as many ants as possible outside the nest entrance and marked them with a one-colour code (one colour for each day). On the following days, we marked the newly arriving ants individually with three colour dots on the thorax and abdomen. The colours allowed us to identify the experimental animals at a distance without capturing them. During the first day of marking ants, the four landmarks were installed around the nest. Two days later, we started to train individually marked ants to visit the feeder. During the experimental period in 1998, a stationary observer was present at the single feeder for the full day and recorded each visit by the individually marked ants at the feeder. Food was presented at the feeder only when the observer was present. This procedure allowed us to record the great majority of the foraging runs performed each day by all marked ants that visited the feeder.
After the ants had visited the feeder, they were captured at the nest, i.e. less than 1 m from the landmark closest to the nest (so-called zero-vector ants) and displaced inside a covered glass vial to a nearby test field where the same landmark arrangement as that present at the nest had been installed. The test field was located in an open area without any nearby landmarks. It covered 30 mx30 m and contained a grid made of thin white lines (grid width 1 m) painted on the ground. The grid was aligned parallel to the northsouth axis.
In the test field, the first search trajectories of the marked ants were recorded after the animals had visited the feeder five times. The ants were released from four different compass directions relative to the landmark array, one of which coincided with the direction towards the feeder (southeast), while the others deviated by ±90 or 180° from this 0° direction (northeast, southwest, northwest). The release sites were located 2 m diagonally from the closest landmark (Fig. 1B). Each ant was tested several times from all four directions. The tests followed each other in random order, with three training-field foraging runs interspersed between individual tests. We released the ants with a piece of biscuit to boost their motivation to home for the fictive nest. The ants' search trajectories were recorded for 3 min each by an observer constantly changing his or her position relative to the searching ant while recording the ants' paths on graph paper.
Data analyses and statistics
The search trajectories of individual ants were digitized on a computer
tablet (MbasaSoft GEDIT; Antonsen, 1995). On the basis of the pooled
trajectories, the search density distributions were calculated for a selected
area (3 mx3 m) around the nest. In Figs
7 and
8, the search densities
pertaining to each experimental configuration are presented both pooled and
separated for all four release sites. We also divided the 3-min tracking
period into two half-periods (1.5 min each). The proportion of the time spent
searching was computed for each of these two half-periods.
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We analysed the number of positions at which the ants searched for the
fictive nest entrance, i.e. where distinct peaks in the search density
profiles occurred. Each search trajectory was evaluated visually, and the
number of positions (0-4) at which the ant had searched for the nest was
classified on the basis of the ants' turning behaviour. If the ant had stopped
and turned at least once within a circle of 20 cm radius around the position
of the hypothetical nest given by the landmark array at any of the four
alternative positions, this was counted as searching for the nest. The
majority of the ants, however, turned a number of times and returned several
times to the same position to search for the nest. The median values resulting
from these computations of the four alternative positions given by the
landmark scene at which individual ants searched for the nest were compared
for different experiments using the median test
(Siegel and Castellan,
1988).
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Results |
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In total, we recorded the search trajectories of 27 individually marked ants (release sites given in Fig. 1B; northwest N=16, northeast N=18, southwest N=20, southeast N=22). On the basis of these search trajectories, we calculated the relative search activities pertaining to all 225 20 cmx20 cm2 pixels of the four-cylinder landmark array (Fig. 2). The search density distribution given in Fig. 2 (southeast) corresponds to searching performed by ants captured and released in the direction of approach from the feeder during training. There is a single high search density peak. In contrast, the search density distributions recorded for ants released at any of the other directions (Fig. 2, northwest, northeast, southwest) resulted in two obvious peaks, one located at the hypothetical geographical position of the nest and a second peak at that of the three other snapshot-matching sites that was closest to the site of release. The great majority of the ants started to search for the nest at the closest hypothetical nest position during the first half of the tracking period (1.5 min) and searched at the correct geographical position of the nest given by celestial and landmark information during the second half of the test period (Fig. 3). This behaviour was especially obvious in releases from southwest and northwest (Fig. 3). In three cases (northwest, southwest and southeast in Fig. 3), search intensities were slightly lower during the second half of the test period.
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Individual ants released from directions different from the training
direction most often searched at two positions [median=2 for all,
N=16 (northwest), N=18 (northeast), N=20
(southwest); Fig. 4]. They
usually changed to the correct position of the hypothetical nest during the
second half of the search period. In contrast, ants released from the
direction of training predominantly searched at only one position [median=1,
N=22 (southeast)], i.e. the correct position of the (fictive) nest
(median test, 2=15.2, d.f.=3, P<0.01;
Fig. 4). Examples of search
trajectories for two ants released from all four directions are given in
Fig. 5. The only direction of
release from which ants (N=2) were recorded never to enter the
landmark array and search for the nest was at the release site northwest of
the landmarks, which is located opposite to the direction towards the feeder
(Fig. 4).
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We also compared the number of positions at which the ants searched for the
nest after different lengths of training: (i) after five to maximally 14
recorded natural foraging runs performed on the same day and (ii) after a
training period lasting for at least 3 days. For individual ants, the mean
number of visits to the feeder was 29.2±27.1 (mean ± S.D.;
N=29) per day (S. Åkesson and R. Wehner, in preparation). These
experiments with different lengths of training were performed to investigate
whether the coupling between landmarks and celestial compass cues becomes
weaker as training time proceeds. Ants of the long-training group, each
trained to one of four different feeders, searched for the nest at more than
one position when released from the direction of training (median=3,
minimum=1, maximum=4, N=26, Fig.
6) compared with ants of the short-training group (southeast, see
above and Fig. 4; median test,
2=13.5, d.f.=1, P<0.001). Furthermore, the number
of positions at which the ants searched for the nest did not depend on the
location at which they had been released (in the training direction or from
any of the other three compass directions) for the group of ants that had been
allowed a training period of at least 3 days (median test,
2=0.007, d.f.=1, P>0.05).
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In a companion training paradigm, the ants had to locate the nest in the
centre of a four-cylinder landmark square. This experiment was designed to
create an unambiguous landmark situation and to test whether in such a
situation an experimental rotation of the landmark array relative to the
celestial system of reference had any effect. The ants searched intensely at
the (only one) fictive position of the nest when released from any of four
alternative compass directions (training landmark array depicted in inset of
Fig. 7; cf.
Åkesson et al., 1998),
and the search density profiles centred at the fictive position of the nest
were only slightly broader when the landmark arrays had been rotated by 45
° (Fig. 8).
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Discussion |
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Ants released at a site coinciding with the direction of training exhibited high search intensities at the fictive position of the nest, demonstrating their ability to learn to use an array of landmarks and to place it correctly into the celestial frame of reference. However, when the same individuals were released from directions other than the direction of training, they most often searched for the nest at two of the four alternative positions within the four-cylinder landmark array: first at the position closest to the point of release, where landmarks and skymarks were out of register, and then at the `true' position of the nest. This behaviour indicates that the memorised landmark image can temporarily be decoupled from the celestial system of reference. An alternative explanation of the ants' search behaviour might be that they perform a stereotyped search by following fixed routes followed by brief pauses and turns. Such search behaviour might at first glance be supported by the observations of ants returning to the nest after short training periods (Fig. 5), in which some ants seem to make a brief pause at the end of the return route rather than following more intense searching and turning at the hypothetical nest. However, a stereotyped search strategy, with fixed routes mixed with brief turning, was not observed for ants recorded after a longer training period (Fig. 6), suggesting that they were indeed searching at the alternative positions of the fictive nest, with the celestial system of reference temporarily decoupled from the landmark image.
Honeybees have been shown to store landmark patterns with reference to
compass cues (Dickinson, 1994;
Collett and Baron, 1994
;
Fry and Wehner, 2002
).
Dickinson (1994
) trained
honeybees to locate the site of a feeder near a cylindrical landmark when the
bees were given access to the natural clear sky during training and testing.
The bees' visits to four alternative positions relative to the landmark were
then recorded; they were able to determine the fictive position of the feeder
only when celestial cues were available, but not when the sky was completely
covered by clouds. These experiments indicate that the bees are able to store
landmark images relative to a celestial system of reference
(Dickinson, 1994
), as
previously suggested by Lindauer
(1960
). However, Collett and
Baron (1994
) reported that
honeybees were able to locate a feeder relative to landmarks even if celestial
cues were absent as long as magnetic cues were available. Their experiments
suggest that the Earth's magnetic field could also provide compass information
for bees.
One could argue that the external system of reference shown to be effective
in our experiments was provided by distant landmarks rather than by skylight
information. In the salt-pan environment, in which the experiments were
performed, this possibility can be almost completely ruled out. As seen from
the nest entrance, the largest (isolated) landmark subtended 0.7°, and the
few isolated landmarks that could be seen in the test field were even lower
and in completely different positions. Hence, in all likelihood, it is a
skymark system that the ants used as a frame of reference in our experiments.
Distant landmark panoramas have been shown to be used as a navigational
guidemark by homing wood ants, Formica japonica
(Fukushi, 2001). However, in
these experiments, the upper skyline of the surrounding trees, which was the
important part of the landmark scene, was much higher (subtending >20°)
than in our experiments (subtending <2°, see also
Wehner et al., 1996
).
Furthermore, in our experiments the configuration of the natural distant
landmarks differed between the training and test areas.
Cartwright and Collett
(1983) made a detailed study of
the characteristics of the reference system by which honeybees use their
memorised landmark panoramas to locate the site of a feeder. They rotated an
asymmetrical array of three landmarks by 30-90° and found that the bees
responded to these shifts by changing their search position only if the
landmarks were rotated by a substantial amount (>45°) relative to the
training configuration. The authors concluded that the bees do define the
landmark scene with respect to external coordinates, but that they do so with
a certain degree of imprecision (Cartwright
and Collett, 1983
). Their findings agree well with our
observations that the search density profile centred above the fictive
position of the nest was only slightly broader when the landmark array had
been rotated by 45° (Figs 7
and 8).
In conclusion, the most important result of the present experiment is that ants can store images of panorama skylines with a celestial system of reference, but that they are also able to decouple their snapshot memories from this frame of reference. The experiments further suggest that this decoupling might be facilitated over time, such that, after some days of training, desert ants prioritize the current landmark memories and to a certain extent ignore the conflicting celestial information experienced when searching for the nest.
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Acknowledgments |
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