The influence of beacon-aiming on the routes of wood ants
School of Biological Sciences, University of Sussex, Brighton, UK, BN1 9QG
* Author for correspondence (e-mail: paulgr{at}cogs.susx.ac.uk)
Accepted 29 October 2002
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: wood ant, Formica rufa, beacon aiming, landmark, navigation, route learning, visual cue
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The arena
Experiments were performed in a 220 cmx300 cm arena that was lit by
four fluorescent strip lights. The arena was surfaced with roughened white
Perspex. Visual cues external to the arena were reduced by a 280 cm-high
curtain that surrounded the arena. One landmark, a black cylinder, 25
cmx50 cm (diameter x height), was placed in the arena. Ants were
carried from the nest on a drinking straw to a small raised starting platform
in the arena, from which they descended by a small ramp to reach the floor. A
feeder (a drop of sucrose solution on a microscope slide) was placed
approximately 300 cm from the starting point. Ants were trained with the
cylinder either to the left or to the right of the direct path from start to
feeder (Fig. 1).
|
Training
At the beginning of training, 20-30 active ants from the colony were placed
on top of the start ramp and the feeder placed at the finish. The first 15
ants to reach the feeder were caught and individually marked with enamel
paint. These ants were then allowed to feed and to return to the start, where
they were caught again and returned to the nest. Ants typically emerged from
the nest mound after a few minutes and were given another training trial.
Tests were introduced after 15 training trials. During the testing phase, ants
were given three rewarded training runs between non-rewarded tests. Between
runs, the arena surface was wiped down with ethanol to remove possible
pheromone cues.
Tracking
The ants' trajectories were tracked with a camera placed 3 m above the
centre of the arena. The camera (Sony EVID30) has movable optics, allowing a
high-resolution image of any part of the arena to be captured. The camera is
controlled by a PC (Pentium II 233 MHz) running custom software
(Fry at al., 2000) that
maintains the ant at the centre of the camera's visual field and stores the
pan and tilt values of the camera at 50 frames s-1. The orientation
of the long axis of the ant is calculated in real time. The 180° ambiguity
is solved by assuming that the ant always walks forwards. Before analysis, the
output was converted to arena coordinates and smoothed by taking a moving
average with a window size of 9 frames. The recordings of trajectories were
cut short when, as often happened, the ant walked close to the cylinder. The
directions of trajectories are measured anti-clockwise relative to the
straight line between the start position and the feeder.
Measuring straightness
The straightness of each trajectory was computed over the first 80 cm of
the route, a distance over which the trajectory could be recorded without
mishap. The method for calculating straightness follows that suggested by
Batschelet (1981). Paths are
broken into small sections recorded at equal time intervals of 1 s. The path
is therefore reduced to a series of unit vectors. The length of the mean
direction of the unit vectors provides a measure of the coherence of their
directions and thus the straightness of the path: the closer the mean vector
(r) is to 1, the straighter is the path.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The first 10 or so trials were not recorded. Trajectories thereafter changed little. Their straightness (see Materials and methods) improved slightly over another 50 trials (regression: r2=0.30, ß=0.175, P<0.01) but there was no change in the overall time taken to reach the food (regression: r2=0.001, ß=-0.026, P=0.8).
The shape of mature trajectories is strongly determined by the position of
the cylinder (Fig. 1). When the
cylinder was on the left, nine out of 10 ants always headed towards it on
leaving the starting position (binomial test, P0.01). The tenth
ant headed slightly right on three occasions but the rest of its 18
trajectories were all oriented left of centre. When the cylinder was on the
right, 10 out of 14 ants headed right towards the cylinder on every
trajectory, two ants headed towards the cylinder on
75% of their
trajectories (binomial test, P
0.01). The remaining two ants
always headed left. These atypical ants are excluded from subsequent
analysis.
Trajectories with the cylinder removed or displaced
After 15 training trials, ants were occasionally tested either with the
cylinder removed or with the cylinder shifted to the equivalent position on
the opposite side of the arena to that used in training. In both conditions,
ants headed roughly in the same direction as they had in training
(Fig. 2). With no cylinder
present, the first 40 cm of the trajectory differed significantly from the
training conditions, with the direction of trajectories rotated a little
further from the direct line from start to feeder than it was in training
(mean heading ± circular S.D., number of trajectories: training:
26.86±10.9°, n=194; no cylinder: 39.5±23°,
n=64; Watson Williams F-test: F256=31.9,
P<0.01). At 80 cm, the heading directions of ants with no cylinder
present were similar to those of ants during training (training:
28.5±12.3°; no cylinder: 30.7±15°;
F256=1.48, P=0.23). However, the differences
earlier in the trajectory mean that, with no cylinder present, ants at 80 cm
continued to head towards the usual position of the cylinder, rather than
turning towards the food, as they did in training.
|
When the cylinder was shifted to the equivalent position on the other side of the arena, ants also headed towards the training position of the cylinder (Fig. 2B). Trajectory headings after 40 cm and 80 cm did not differ significantly from those performed during training (after 40 cm: training: 26.86±10.9°, n=194; cylinder in opposite position: 32.4±29°, n=21; Watson Williams F-test: F213=2.7, P=0.1; after 80 cm: training: 28.5±12.4°; cylinder in opposite position: 27.4±26°; Watson Williams F-test: F213=0.1, P=0.8).
Although the direction of mature trajectories was not much influenced by removing or displacing the cylinder, both the speed and the straightness of the trajectories were reduced. Ants took significantly longer to reach 80 cm when there was no cylinder in the arena. (mean ± S.D., number of trajectories: training: 54±32 s, n=194; no cylinder: 74.4±42 s, n=71; MannWhitney test: U=5379, Z=-4.5, P<<0.01) or when the landmark was displaced (training: 54±32 s, n=194; displaced cylinder: 89.0±62 s, n=22; MannWhitney test: U=1403, Z=-3.5, P<<0.01). The mean walking speed of ants in the two test conditions was slightly but significantly lower than it was in training (training: 2.8±0.89 cm s-1; no cylinder: 2.48±0.58 cm s-1; displaced cylinder: 2.49±0.69 cm s-1; t-test pooled across test types, d.f.=263, t=3.1, P<0.01). The trajectories during these tests were significantly less straight than in training (training: 0.71±0.17; no cylinder: 0.52±0.16; displaced cylinder: 0.43±0.18; one-way ANOVA: F2,294=4.7, P<<0.005; post-hoc comparisons: training vs no cylinder and training vs displaced cylinder, P<<0.005).
What maintains trajectory shape when the cylinder is missing?
To understand better what preserves the shape of the ant's route when the
cylinder is removed, ants were tested with no cylinder present and with the
start position displaced by 30 cm to the left or to the right of the usual
start position. The ants' trajectories in these conditions were compared with
those in tests with no cylinder when started from their normal position. Ants
that were started 30 cm away from the normal start position still headed
towards the usual position of the cylinder. Data from ants trained with the
cylinder on the left or the right were combined and the two test conditions
are referred to as `near start' and `far start', referring to the distance of
the start position from the cylinder (Fig.
3).
|
The trajectory headings of ants started from the near and far positions differ significantly from those with normal starts at 40 cm, 60 cm and 80 cm from the start (see Table 1). The mean headings in the far condition are rotated further away from the direct line from start to feeder than with normal starts, and the headings in the near condition do not rotate as far. At all three distances from the start, the directions of the normal, near and far trajectories tend to converge towards the usual position of the cylinder (Fig. 3). The areas of convergence are represented by the open triangles on Fig. 3.
|
The data are consistent with the ant moving towards a point in the arena
that is familiar to them from their training runs. Two possibilities can be
rejected. The data are not consistent with ants having learnt to take a
particular direction from the start, as given, for instance, by a constant
angle relative to the strip lights on the ceiling (cf.
Hölldobler, 1980). Nor do
the data suggest that ants first head towards their normal start position. We
suggest that the ant has stored a view of the room from the position of the
landmark. As the arena floor is featureless, this view is most probably based
on more-distant landmarks such as the lighting array, folds in the curtain and
contrast boundaries where the curtains meet the ceiling.
Retinal position of the cylinder during the ants' approach
An analysis of where the cylinder was placed on the ant's retina during the
trajectories, as estimated from the orientation of the ant's longitudinal
axis, is shown in Fig. 4A. The
mean retinal positions of the centre and of the `left' and `right' edges of
the cylinder, from the ant's viewpoint, are plotted for the first 80 cm of the
trajectories. Over the first 45 cm, the cylinder shifts from `right' frontal
retina to the centre of the eye (Fig.
4C), where it appears to be fixated for a short spell
(approximately 10 cm). The cylinder then shifts further to the left and the
`right' edge is held stably on frontal retina
(Fig. 4D). After about 65 cm,
the ant turns towards the feeder.
|
The same analysis can be performed on trajectories from the tests in which
the cylinder was removed or displaced. In this case, one calculates the
retinal position of an imaginary cylinder placed in the usual position of the
real one. There are two major differences between the paths of imaginary and
real cylinders over the retina (Fig.
4B). First, the spread of retinal positions is much narrower when
a real cylinder is present than in its absence. Second, ants head towards the
imaginary cylinder for longer before turning towards the food than they do
when the cylinder is present. These differences suggest that the sight of the
cylinder fine-tunes the ant's trajectory in two ways. It first acts as a
beacon that the ant fixates in different ways (cf.
Nicholson et al., 1999) and it
then signals that the ant should turn in the direction of the feeder (cf.
Collett et al., 1992
).
Training with more-distant cylinders
Two additional groups of ants were trained with the same sized cylinder
placed 2 m from the start line and 60 cm from the direct line from start to
food (Fig. 5). Despite its
increased distance from the start, the cylinder continued to attract ants. The
trajectories of 10 out of 11 ants were biased towards the side of the arena
containing the cylinder (binomial test P<<0.01). But the
trajectories were less tightly clustered than they were when the cylinder was
closer. Individual ants developed idiosyncratic routes that were consistent
across trials (Fig. 5A-C). With
the cylinder less prominent, it seems likely that, during learning, ants were
also attracted by other visual features of the arena. The paths of the ant in
Fig. 5A, for instance, suggest
that this ant has learnt to aim at some feature of the side wall before
turning towards the cylinder. That different ants appear to be channelled by
different, rather unobtrusive, visual features suggests that when an ant's
attention is momentarily captured by a particular feature at the start of
route acquisition, that feature is rapidly learnt and continues to guide the
ant on subsequent trips. Like those of ants trained with the landmark in the
closer position, the ants' paths had roughly the same shape when the cylinder
was removed (Fig. 5D-F). The
difference in clustering between the closer and more-distant cylinder is shown
in Fig. 5G-J, which plots the
mean trajectory of each ant trained with the cylinder at 1 m or 2 m from the
start. We calculated the distances between mean directions for individual ants
after 80 cm and the mean direction of all trajectories within that condition.
The paths of ants trained with the cylinder at 2 m are significantly more
dispersed than those of ants trained with the cylinder at 1 m (mean ±
95% confidence, number of ants: 1 m: 4.9±2°, n=15; 2 m:
11.2±6°, n=10; Watson's F-test:
F23=5.92, P=0.02).
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Of particular significance is the finding that if ants are displaced away
from the route, in the absence of the cylinder, they are not attracted to the
closest point along the route but rather to where the cylinder is normally
found (Fig. 3). This position
seems to have been learnt as an intermediate goal. Perhaps the extra visual
cues that are learnt comprise a snapshot taken at the site of the cylinder.
This finding adds significantly to the body of evidence suggesting that
insects are pre-disposed to partition routes into segments, using landmarks to
define the boundaries between segments (e.g.
Collett et al., 2002). It
suggests further that memory acquisition is particularly abundant at segment
boundaries.
In addition to supporting the ant's navigation to the beacon, it is likely
that the putative snapshot taken at the site of the cylinder provides a
contextual cue that can prime an ant's memory of the cylinder and so increase
the reliability of its recognition (cf.
Collett and Kelber, 1988;
Collett et al., 1997
). In
general, accurate recognition of a beacon is important because particular
actions are associated with particular beacons turning towards the
feeder in this case. Contextual support for accurate recognition may well be
essential along more natural, longer routes, if several rather similar
discrete beacons must be distinguished or if the ant's path is noisy and it
approaches a beacon from an unusual direction. Its atypical context may
explain why the ants tended to ignore the cylinder when it was moved to an
unusual position.
It is instructive to compare the present results with the way that desert
ants and wood ants treat extended landmarks
(Collett et al., 2001;
Graham and Collett, 2002
). If
ants can obtain continuous landmark information along the route from an
extended landmark, like a wall or a dense row of plants, their path is less
constrained by the landmark and they can learn a variety of paths relative to
this landmark. They learn the appearance of a wall along their chosen route in
terms of the retinal elevation of the top of the barrier at different points
along it (Pratt et al., 2001
,
Graham and Collett, 2002
) and
they then adjust their path to keep the barrier at the learnt
elevation(s).
In the case of desert ants, ants homed from a feeder around a 10 m barrier
that was positioned perpendicularly to the direct route. On rounding the
barrier, the ant's path was initially driven by the global homewards vector
that directed the ant from the end of the barrier straight to the nest site
along a path at an angle of approximately 34° to the barrier. Once the
appearance of the barrier along the route had been learnt, ants followed the
same route relative to the barrier, when the barrier had been rotated through
45°, and the ants were placed at the end of the barrier after nearly
reaching the nest entrance on their return. Ants will thus follow a consistent
path relative to a barrier, despite the absence of useful information from
path integration or the sky compass
(Collett et al., 2001;
Graham and Collett, 2002
).
Information that was essential to learning the path can thus be dispensed with
once the route is familiar. We have shown here that beacons, like path
integration, can act as a scaffold during route learning. The beacon must be
present for ants to learn a particular route. But, once the route has been
acquired, this scaffold can be omitted without seriously degrading the shape
of the route.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Batschelet, E. (1981). Circular Statistics in Biology. London: Academic Press.
Chittka, L., Kunze, J., Shipman, C. and Buchman, S. L. (1995). The significance of landmarks for path integration of homing honey bee foragers. Naturwissenshaften 82,341 -343.[CrossRef]
Collett, M., Collett, T. S., Bisch, S. and Wehner, R. (1998). Local and global vectors in desert ant navigation. Nature 394,269 -272.[CrossRef]
Collett, M., Harland, D. and Collett, T. S.
(2002). The use of landmarks and panoramic context in the
performance of local vectors by navigating honeybees. J. Exp.
Biol. 205,807
-814.
Collett, T. S. (1988). How ladybirds approach nearby stalks: a study of visual selectivity and attention. J. Comp. Physiol. A 163,355 -363.
Collett, T. S. and Baron, J. (1994). Biological compasses and the coordinate frame of landmark memories in honeybees. Nature 368,137 -140.[CrossRef]
Collett, T. S., Collett, M. and Wehner, R.
(2001). The guidance of desert ants by extended landmarks.
J. Exp. Biol. 204,1635
-1639.
Collett, T. S., Dillmann, E., Giger, A. and Wehner, R. (1992). Visual landmarks and route following in desert ants. J. Comp. Physiol. A 170,435 -442.
Collett, T. S., Fauria, K., Dale, K. and Baron, J. (1997). Places and patterns a study of context learning in honeybees. J. Comp. Physiol. A 181,343 -353.[CrossRef]
Collett, T. S. and Kelber, A. (1988). The retrieval of visuo-spatial memories by honeybees. J. Comp. Physiol. A 163,145 -150.[Medline]
von Frisch, K. (1967). The Dance Language and Orientation of Bees. London: Oxford University Press.
Fry, S. N., Bichsel, M., Muller, P. and Robert, D. (2000). Tracking of flying insects using pan-tilt cameras. J. Neurosci. Meth. 101,59 -67.[CrossRef][Medline]
Fry, S. N. and Wehner, R. (2002). Honey bees store landmarks in an egocentric frame of reference. J. Comp. Physiol. A 187,1009 -1016.[Medline]
Götz, K. G. (1994). Exploratory strategies in Drosophila. In Neural Basis of Behavioural Adaptations, Fortschritte der Zoologie vol.39 (ed. K Schildberger and N. Elsner), pp.47 -59. Stuttgart: Gustav Fischer.
Graham, P. and Collett, T. S. (2002).
View-based navigation in insects: how wood ants (Formica rufa L.)
look at and are guided by extended landmarks. J. Exp.
Biol. 205,2499
-2509.
Hölldobler, B. (1980). Canopy orientation: a new kind of orientation in ants. Science 210, 86-88.
Judd, P. D. and Collett, T. S. (1998). Multiple stored views and landmark guidance in ants. Nature 39,710 -714.
Nicholson, D. J., Judd, P. D., Cartwright, B. A. and Collett, T.
S. (1999). Learning walks and landmark guidance in wood ants
(Formica rufa). J. Exp. Biol.
202,1831
-1838.
Poteser, M. and Kral, K. (1995). Visual distance discrimination between stationary targets in praying mantids: an index of the use of motion parallax. J. Exp. Biol. 189,2127 -2137.
Pratt, S., Brooks, S. E. and Franks, N. F. (2001). The use of edges in visual navigation by the ant Leptothorax albipennis. Ethology 107,1125 -1136.[CrossRef]
Rosengren, R. (1971). Route fidelity, visual memory and recruitment behaviour in foraging wood ants of genus Formica (Hymenopterus, Formicidae). Acta Zool. Fenn. 133,1 -106.
Santschi, F. (1913). Comment s'orientent les fourmis. Rev. Suisse. Zool. 21,347 -425.
Srinivasan, M. V., Zhang, S. W. and Bidwell, N. J.
(1997). Visually mediated odometry in honeybees navigation en
route to the goal: visual flight control and odometry. J. Exp.
Biol. 200,2513
-2522.
Strauss, R. and Pichler, J. (1998). Persistence of orientation toward a temporarily invisible landmark in Drosophila melanogaster. J. Comp. Physiol. A 182,411 -423.[CrossRef][Medline]
Wallace, G. K. (1962). Experiments on visually controlled orientation in the desert locust, Schistocerca gregaria (Forskål). Anim. Behav. 10,361 -369.
Wehner, R. (1972). Spontaneous pattern preferences of Drosophila melanogaster to black areas in various parts of the visual field. J. Ins. Physiol. 18,1531 -1543.[Medline]
Wehner, R., Michel, B. and Antonsen, P. (1996).
Visual navigation in insects: coupling of egocentric and geocentric
information. J. Exp. Biol.
199,129
-140.