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First published online August 30, 2006
Journal of Experimental Biology 209, 3677-3684 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02414
Bi-directional route learning in wood ants
School of Life Sciences, University of Sussex, Brighton, BN1 9QG, UK
* Author for correspondence (e-mail: T.S.Collett{at}Sussex.ac.uk)
Accepted 27 June 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: wood ant, Formica rufa, view-based navigation, route learning, visual landmarks
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Kohler and Wehner, 2005;
Macquart et al., 2005;
Wehner et al., 1996).
Furthermore, ants will follow the same route irrespective of the state of
their path integration system (Andel and
Wehner, 2003; Kohler and
Wehner, 2005; Wehner et al.,
1996). When displaced from the feeder or nest to a point midway
along the route, they immediately join the route and continue it to its end
(Kohler and Wehner, 2005). A
different kind of evidence for visual route guidance comes from observing how
an acquired route depends on the distribution of visual features within an
ant's environment (Graham et al.,
2003) and how displacing, changing or removing visual landmarks
after a route has been acquired influences an individual's path
(Collett et al., 1998;
Collett et al., 1992;
Collett et al., 2001;
Graham and Collett, 2002;
Macquart et al., 2005).
Visually guided food-bound and homeward routes can be very similar
(Santschi, 1913), but they can
also differ (Kohler and Wehner,
2005; Macquart et al.,
2005; Wehner et al.,
1983); [also see fig. 7B,C in
(Wehner, 2003)]. In either
case, ants travelling in the two directions, between their nest and food or
their food and nest, encounter and learn different sequence of views and
associate different actions with those views. When there is a distinct spatial
separation between food-bound and homeward routes
(Wehner et al., 2006), visual
information pertaining to the food-bound or homeward route must be acquired
while performing that route. When the two routes are similar, the question
arises as to whether ants might acquire landmark information to guide their
homeward route on their food-bound route and vice versa. Such
cross-route learning would help make food-bound and homeward routes more
similar, which would be useful in some environments, and might speed up route
learning. It would also enhance the opportunity for communication between ants
travelling in opposite directions. One might expect cross-route learning to be
particularly prevalent in ant species that are guided along trails by a
combination of chemical and visual cues and so may tend to follow the same
path in both directions.
In the first part of this paper we examine whether information for guiding a wood ant's homeward route can be acquired on the ant's outward route. The basic experimental design was to give ants ample experience of a food-bound route, but to prevent any experience of a homeward route. We then examined whether these ants, which were only accustomed to travelling towards the food, could nonetheless perform elements of a homeward route.
In the second part of the paper, we examine the way that food-bound and homeward routes develop by recording the successive food-bound and homeward trips performed by individual ants. Is there a close similarity in the evolution and final form of an individual's food-bound and homeward routes? To test whether running a homeward route facilitates acquisition of a food-bound route, we compared the developing food-bound routes of ants that were and were not allowed to run their homeward routes.
Navigational learning in insects is to a large degree anticipatory in the
sense that insects learning a visually guided route are programmed to acquire
relevant visual information at particular points along the route. The best
understood behavioural routines aiding acquisition are the elaborately
structured learning flights that bees
(Lehrer, 1993) and wasps
(Collett and Lehrer, 1993;
Tinbergen, 1932;
Zeil, 1993) perform when they
first leave a significant place to which they will return, such as their nest
or a newly discovered feeding site. The probable function of these localised
flights is to allow an insect to pick up appropriate information that can
guide its later return to the place. A failure to execute a learning flight
can lead to difficulties when the insect tries to find that goal on its return
(Lehrer, 1993;
Wagner, 1907). Wood ants, too,
have been found to look back and approach nearby landmarks after they have
found a new source of food (Judd and
Collett, 1998; Nicholson et
al., 1999; Rosengren,
1971). Desert ants behave similarly when first leaving their nest
(Wehner et al., 2004). But
little is known about whether and where ants turn and look backwards along a
route.
In the third section of the paper, we analyse the wood ant's food-bound and
homeward routes to identify where information for guiding the opposite paths
might be acquired. Because the landscape will generally look different in the
two directions, ants are likely to learn landscape features for guiding their
path in the reverse direction at times when they have turned around and are
retracing their steps. If such potential points of acquisition do occur, how
are they distributed along the ants' paths? Large landmarks act as beacons and
seem to form intermediate goals that sub-divide a route [for bees
(von Frisch, 1967); wood ants
(Graham et al., 2003)], so
that an interesting possibility is that turn-backs are particularly common
close to a landmark that serves as an intermediate goal. A second question to
be examined is whether turn-backs occur mostly in early routes, when ants are
still inexperienced.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). To
select ants for training, a group of potential foragers was taken from the
nest and placed at the start of the route. The first 20 or so ants to reach
the food site through random search were caught and then marked individually
with two dots of enamel paint (Humbrol, UK). These ants constituted an
experimental group. Usually, about two-thirds of the group foraged
consistently and could be trained.
The arena
Two experiments were conducted within low-walled rectangular arenas (see
Fig. 1A) the floors of which
were covered with large (A0) sheets of white paper that were changed regularly
to eliminate scent cues. The arena for the first experiment was 168
cmx94 cm, and the arena for the second experiment was 200 cmx124
cm. These arenas were placed at the centre of a larger curtained area (280
cmx380 cm) illuminated by banks of high frequency fluorescent lights
concealed above a translucent plastic ceiling. The floor-to-ceiling curtains
were white on three sides and were decorated with large black shapes on the
fourth side (Fig. 1A). Ants
followed a two-legged outward route from one end of the arena (S) to a food
site (F) at the other end of the arena. The first leg of the route was along
an open-topped narrow channel, 10 cm wide, with 10 cm high solid
white-finished walls. A black cylinder (47 cm high and 15 cm diameter)
straddled the channel at the end of the first leg of the route. The channel
prevented ants from seeing the overall position of the cylinder in the room
until they had passed the cylinder. The second leg of the route extended from
the channel exit across the open arena to the food site. A concealed tracking
camera mounted in the ceiling recorded the paths of individual ants
(Fry et al., 2000;
Graham and Collett, 2002).
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After about 20 outward trips, each ant was given the opportunity to perform
a homeward route. To avoid any possible bias due to path integration, the ant
did not make its own way to the feeder. It was taken from the nest and placed
adjacent to a drop of sucrose on a microscope slide that was located at floor
level in the usual position of the feeder. Ants were not disturbed by this
unexpected procedure and mostly began feeding straight away. Two identical
cylinders were placed in the arena. One cylinder was in the training position
and the other in a mirror symmetric position on the other side of the direct
path between start and feeder (Figs
1 and
2). Graham et al. showed that
wood ants, during route learning, memorise both the appearance of a local
landmark and the surroundings in which the landmark is set
(Graham et al., 2003). They
tend to ignore familiar looking landmarks placed in an inappropriate context.
Therefore the extra landmark, whilst balancing out any innate landmark
attraction, should not disrupt any manifestation of a learnt homeward route.
The arena floor was covered with fresh paper to eliminate guidance by chemical
trails and the channel was removed so that the arena configuration was
symmetrical.
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Route analysis
The bias of each individual trajectory to one or other side of the arena
was assessed by calculating the mean position on the horizontal (x)
axis - with the feeder at x=0. Trajectories were said to be biased to
the left if the mean x position was <0 and to the right if the
mean x position was >0.
To obtain an overall measure of how routes change with experience, we
computed two global characteristics of each ant's path, first its straightness
and second its consistency with respect to the preceding path of the same ant.
In order to measure straightness, the recorded path was divided into multiple
sections of equal duration (2 s) and the heading of each section was
calculated. The straightness of the trajectory is then given by the coherence
of these headings (Batschelet,
1981). A value of one indicates a straight path and a value of
zero indicates a path with no overall direction (e.g. a circle).
The consistency between pairs of consecutive trajectories was estimated by a procedure in which we first calculated the area enclosed by the two trajectories by counting the number of 1 cm grid squares that were enclosed by the paths or through which the paths passed. This value was then normalised by dividing it by the combined length of the paths. This procedure gives a minimum value of 0.5 when the paired trajectories are identical.
To assess the statistical significance of any changes in consistency and straightness, runs were grouped into three successive blocks of 10, and the mean straightness and consistency of the runs were computed for each individual over each block and the scores analysed with a repeated-measures ANOVA.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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We measured and compared the straightness and distance of the ants' paths for each run and found no significant differences between the first and second test runs (Sinuosity; mean ± s.d.: first runs, 0.30±0.27; second runs, 0.27±0.24; Student's t-test; P=0.65, t=0.46, d.f.=49: Maximum distance reached; mean ± s.d.: first runs, 63±30 cm; second runs, 61±28 cm; Student's t-test; P=0.76, t=0.30, d.f.=49).
Half of the ants were trained with the channel and cylinder to the left of the direct line from the start to the feeder, for the other half the channel and cylinder were to the right of that line (Fig. 1A,C). The superimposed test trajectories for each of these training conditions are shown as separate density plots in Fig. 1B,D. Both plots are biased significantly towards the side where the channel and landmark had been during outbound runs. The return journeys of ants from both training conditions were biased significantly toward the position of the channel in training. Most (17/23; sign test, P=0.017) trajectories from ants trained with the channel to the right of the direct line to the feeder were biased to the left. Whereas most (21/28; sign test, P=0.006) trajectories from ants trained with the channel to the left were biased to the right.
The individual test trajectories are shown in Fig. 2A, with the paths of the right-trained ants mirrored to make them compatible with those of the left-trained ants. For clarity, a solid-circle marks the end-points of each recorded track. The end-positions are not behaviourally significant, as the tracks often stopped when the 6 min recording time was over, or before, if the tracking camera became locked onto the cylinder or the sidewall of the arena. Ants rarely took a direct path to the cylinder. Usually, they just moved somewhat erratically on the correct side but `above' the channel exit, as they often did in early foraging trips when allowed to return home normally (Fig. 3). The ants' erratic movements can also be seen in Fig. 2B-D, which shows with a dot where each trajectory crossed circles of 20, 40 and 60 cm radius centred on the feeder.
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Looking back along food-bound and homeward routes
Ants on the food-bound or homeward leg of their foraging route can give
themselves an opportunity of acquiring views for guiding travel in the reverse
direction by turning around and retracing their steps for a short segment. We
scanned the recorded routes for reversals of this kind to discover when and
where reversals occurred and how long they were. We looked for path segments
in which the ants turned around and faced within ±20° of the
cylinder at the end of the channel on food-bound routes or within
±20° of the feeder on homeward routes.
Reversals on the food-bound path
Occasionally, when ants were already some distance away from the channel
exit, they reversed direction, returned to the channel exit and re-entered the
channel. They then usually re-emerged to walk to the feeder. Loops at the
start of food-bound routes occurred on about 25% of early runs and became
rarer as ants became experienced with the route. None occurred after run
12.
More frequently, ants turned back, retraced their path for a short segment and then continued with the food-bound segment. Twenty-seven out of 29 trained ants reversed direction at least once. Reversals were usually marked by the ant looping or making a U-bend (e.g. Fig. 5A). Most reversals were less than 3 cm long (25th, 50th and 75th percentile of the distribution were 0.966, 2.450 and 8.387 cm, respectively, N=92). Reversals occurred more often in early than in later runs (Fig. 5B) and were distributed evenly along the path (Fig. 5C). The occurrence of brief U-bends and loops on relatively straight segments is consistent with the suggestion that the reversals are performed to acquire landmark information and that they are not just a by-product of the ant's erratic path on early trials.
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On early runs ants often moved away from the feeder and looped back after a
short excursion before eventually making a full homeward trip. These loops
could be in any direction and were not biased towards the exit to the channel.
As reported earlier for learning flights in wasps
(Zeil, 1993) and also for
similar loops in wood ants (Nicholson et
al., 1999), these loops often occur on the first runs of each day,
even in well-trained ants (Fig.
5G).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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What did ants acquire during their previous outbound trips that might guide their homeward segments? By testing ants after they were carried to the feeder, we eliminated the possibility that ants just reversed their immediately preceding food-bound trip, either using path integration or by reversing their compass direction. It also seems unlikely that the ants stored the overall compass direction of their habitual outbound trip and then after feeding reversed that direction on their first permitted homeward trip.
We suggest that in the tests ants guide their homeward path using views that include the rough location of the cylinder, which they have stored on earlier food-bound trips. Because ants cannot see the location of the cylinder from within the channel we suppose that the ants were guided by directional views acquired between the exit from the channel and the food site, and that these views were acquired when ants were facing roughly in the direction of the channel. The third section of the Results contains evidence that ants do reverse direction on this segment of their outward trip, particularly when they are inexperienced.
As outlined in the Introduction, there is clear evidence that bees and
wasps acquire information to guide their return to a goal when leaving it.
However, the only study to examine when ants acquire homeward route
information (Bisch-Knaden and Wehner,
2003) concluded that the desert ant Cataglyphis fortis
learns homeward local vectors (Collett et
al., 1998) only on the homeward journey and not on the food-bound
journey. Ants, in the Bisch-Knaden and Wehner study, experienced an array of
landmarks close to the feeder either when they approached the feeder from the
nest or only when they left the feeder to return to the nest. To accomplish
this separation, ants were caught at the feeder and carried to a distant site
where they performed a homeward trip driven by their path integration home
vector. They were caught and returned to the nest as soon as they began to
search at the end of their home vector. Each ant was trained over five round
trips of this kind before it was tested. For testing, the ant was caught at
the end of the home vector and replaced at the departure point. This
manipulation ensured that the ants had no global vector and would only move in
a defined direction if a response were to be triggered by the landmarks. Ants
accustomed to viewing landmarks on their way home exhibited a local
homeward-directed vector by travelling a few metres in the direction of their
nest. Ants accustomed to landmarks on the way to the feeder searched around
the release point in an undirected fashion, as did ants trained either with no
landmarks or with landmarks on both routes and then tested with no
landmarks.
The methodologies of the Cataglyphis and Formica
experiments differ in the sense that the wood ants had no experience of a
homeward route before testing, whereas the desert ants were trained without
landmarks on their homeward route and so could have learnt associations that
competed with any reaction to the test landmarks acquired on the food-bound
trip. The barren terrain makes interference of this kind unlikely, and the
more plausible account is that given by Bisch-Knaden and Wehner, that
landmark-induced local vectors are only learnt in the behavioural context in
which they are used (Bisch-Knaden and
Wehner, 2003). By contrast, the current wood ant data suggest that
visual cues to guide the homeward trip may be acquired when ants are in a
food-bound motivated state.
If ants travelling their food-bound route acquire views for guiding both
their food-bound route and their homeward route, how do they know which of the
two sets of stored views they should apply on the way home? Ants must in some
manner label memories as being appropriate either for the way out or for the
way home. Wood ants, which are familiar with a visually guided route, prime
visual memories for their food-bound or homeward trip according to whether
they are unfed or have fed (Harris et al.,
2005). Similarly, a homeward bound Melophorus ignores its
food-bound route if placed on it, but will immediately join its homeward route
(Wehner et al., 2006). The
current data suggest that a wood ant, on acquiring a view on the way to a food
site, tags the view as food-bound or homeward according to whether the view is
acquired when the ant is facing or moving in the direction of food or
home.
One puzzling feature of our data is that it took many trials for the
homeward route to straighten. Two possible reasons for the slow development of
homeward routes are: (1) The learning of homeward routes relies on path
integration more than food-bound routes, and the necessary compass information
to sustain path integration is missing in these laboratory experiments. It is
worth testing if routes are acquired more rapidly outside and if sky compass
cues make it easier for an ant to determine whether a view acquired on the
food-bound route should be pigeonholed as information for guiding future
food-bound or homeward trips. (2) Segments of routes close to the goal may be
learnt faster than more distant segments. In the present experiments, the
monitored part of the route consists of the last segment of the food-bound
route, but the first segment of the homeward route. However, there is some
evidence from bees and ants for a difference in what is acquired on outbound
and homeward routes. Honeybees may learn local vectors on their outward but
not on their homeward routes (Srinivasan
et al., 1997), and data from a recent study on Formica
japonica navigating out of doors
(Fukushi and Wehner, 2004)
hints that outward routes may be learnt better than homeward ones.
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