Do familiar landmarks reset the global path integration system of desert ants?
1 Department of Zoology, Michigan State University, East Lansing, MI 48824,
USA
2 School of Biological Sciences, University of Sussex, Brighton BN1 9QG,
UK
3 Laboratoire Ethologie Expérimentale et Comparée, CNRS
FRE 2413, Université Paris Nord, 99, avenue Jean-Baptiste
Clément, 93430 Villetaneuse, France
4 Department of Zoology, University of Zürich, Winterthurerstrasse 190,
CH-8057 Zürich, Switzerland
* Author for correspondence (e-mail: t.s.collett{at}sussex.ac.uk)
Accepted 26 November 2002
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Summary |
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Key words: familiar landmark, memory, global path integration system, desert ant, Cataglyphis fortis
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Introduction |
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Insects can have long-term memories of global PI information. A desert ant
taken while foraging at a permanent feeder and held in darkness for 24 h
appears to retain some memory of a home vector
(Ziegler and Wehner, 1997).
That honeybees have long-lasting PI memories can be deduced from the
occasional spontaneous dances that bees performed in the middle of the night,
signalling feeder sites that they had visited the previous day
(Lindauer, 1960
). There is
reason to believe that honeybee global PI memories may be cumulative, by which
we mean that through visiting a site over many occasions, a long-term PI
memory may be gradually refined or reinforced. The best evidence comes from an
intriguing `catchup' phenomenon (Lindauer,
1963
; von Frisch,
1967
; Gould, 1984
;
Dyer, 1987
). If bees are
trained to a feeder along a route marked by prominent landmarks, and then the
feeder and landmarks are shifted to make an angle of 30° with the initial
route, the waggle dances indicating the feeder do not shift suddenly. Instead,
at first the dances continue to signal the initial feeder position, and then
over a period of 40 min the direction signalled by the dance shifts gradually
to indicate the displaced feeder position. This gradual catch-up has been
interpreted to reflect a running average of the global PI values at the feeder
position over the previous 40 min period
(Lindauer, 1963
;
von Frisch, 1967
;
Gould, 1984
), although other
interpretations of the data are possible. Such gradual updating would suggest
a cumulative global PI memory of the feeder position. The present work
addresses whether a cumulative global PI memory might exist in desert ants
and, if so, whether such a cumulative global PI memory is associated with
landmark memories and can be recalled when the associated landmarks are
viewed. Our experiments were designed to test whether such a putatively
recalled cumulative memory is used to reset the global PI system to its
accustomed state at a recognised location.
When considering PI memories, it is important to distinguish between global
and local PI vectors. Both ants and bees store views of landmarks in the
immediate neighbourhood of a feeding site
(Anderson, 1977;
Cartwright and Collett, 1983
;
Wolf and Wehner, 2000
). On a
familiar route, these insects can link the memory of a landmark to a memory of
the direction and/or distance of the subsequent path segment
(Collett et al., 1993
;
Srinivasan et al., 1997
). A
`local vector', reflecting a short path segment, can be triggered by a
landmark at the beginning of the segment (Collett et al.,
1993
,
1996
,
1998
,
Srinivasan et al., 1997
), or
by the completion of the previous path segment
(Collett et al., 1993
).
Guidance of local vectors is likely to involve PI
(Srinivasan et al., 1997
), and
appears to use the same environmental cues as global PI, both for the
directional (Collett et al.,
1998
) and distance (Srinivasan
et al., 1997
) components. Unlike the global vectors that are
observed when foragers are displaced to unfamiliar territory, local vectors
seem only to be expressed within the appropriate panoramic context of the
route segment (Collett et al.,
2002
). In the appropriate context, recognition of a familiar
landmark may trigger a cumulative PI memory
(Chittka et al., 1995
), but
current data suggest that it would be a local PI vector of the next path
segment, not the global PI vector that is recalled
(Collett et al., 1998
).
A number of studies have already investigated whether a desert ant that
experiences familiar views along a habitual route segment will recall a
cumulative global PI memory and use the recalled memory to reset its global PI
system to the habitual state at the recognised location
(Sassi and Wehner, 1997;
Collett et al., 1998
; ?.
Bisch-Knaden and R. Wehner, manuscript submitted). In these studies, ants were
trained along a route marked by fixed landmarks, so that the recognition of a
specific landmark could be associated with a particular state of the ant's
global PI system. For tests, the trajectory was altered, so on reaching a
familiar landmark on the homeward route an ant would have an unaccustomed
global PI state. The question asked was whether the act of recognising a
familiar landmark would cause the global PI system to be reset to its
accustomed state on encountering the landmark. The mismatch between landmark
position and accustomed global PI state at the landmark was achieved in three
ways. In one, the foodward route was altered
(Sassi and Wehner, 1997
). In a
second, the foodward route was normal and the homeward route was altered
(Collett et al., 1998
). In a
third, the ants were made to repeat the homeward trajectory after being
captured near the nest at the end of a normal homeward trajectory
(Collett et al., 1998
). In both
the last two conditions the landmarks elicited the performance of local
vectors, so it was clear that the ants recognized the landmarks. Nevertheless,
none of these studies found any evidence that the global PI system had been
reset by the landmarks.
The results of the previous studies suggest that familiar landmarks on the way home do not trigger or reset a homeward global vector. They still leave open the question of whether landmarks on the foodward route, or arrival at a familiar food site, might be used to reset the global PI system or trigger the recall of a homeward global vector. The aim of the present experiments was to answer this question. Ants were trained to a feeder along channels in an L-shaped route. The second half of the route was conspicuously marked with landmarks. After extensive training along this route, ants were given an altered route with the same conspicuous landmarks in the second half, but with the first half lengthened or shortened to change the overall length of the route. The ants' homeward trajectories were then recorded on an open test field to see whether the trajectories reflected the trained or the altered route. If a forager resets its global PI system using a cumulative PI memory associated with the familiar food site, then the homeward global vector would reflect the trained rather than the altered route. If the homeward vectors instead reflect the altered routes, it would indicate that a cumulative global PI memory is not used for the homeward trajectory.
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Materials and methods |
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To promote recognition we used both a right-angle change in direction, and a sequence of landmarks consisting of open buckets that joined sections of channelling. Two openings were cut at the bottom of the wall of each bucket into which the ends of two lengths of channel were inserted. Ants were able to view the outside of a bucket while approaching it along the channel, and then see the inside walls on entering the bucket. The bottom of each bucket was packed with sand giving an additional tactile difference between the plastic floor of the channel and the sandy floor of the bucket. The use of channels and artificial landmarks made it possible to shorten or lengthen the first leg of the route, but still give ants exactly the same visual and tactile experience when they walked along the second part of the route.
To make it easy to collect ants for testing, the channel was connected to the feeder via a one-way system. The channel ended in a plastic box from which ants could enter a tube leading to a feeder bucket. The tube protruded through a hole in the side of the feeder bucket, about 10 cm above the bottom, so that ants had to drop into the bucket to reach a piece of ripe watermelon. The sides of the bucket were coated with fluon, so that the ants could not climb up again to the entrance hole. Instead, to leave, there was an exit tube at the bottom of the bucket that returned them to the plastic box. The separate entrance and exit tubes meant that, in tests, the exit tube could be blocked and ants trapped within the feeding bucket.
Routes A and B
For two nests, polyethylene tubes connected the enclosed nest to the
plastic channels. These channels were flat-bottomed with sloping sides and had
a lip at the top to prevent escape. From the middle of the channel, ants had a
90° view of the sky. The routes started with a length of channel leading
into the first bucket. For nest A the length of this channel was 7 m and for
nest B it was 3 m. Thereafter the routes were the same for the two nests. A
further 1 m of channel from this bucket led in the same direction to a corner
bucket. The first leg of the L was thus 8 m for route A and 4 m for route B.
The second leg of the route from the corner bucket comprised 4 m of channel at
right angles to the first.
While a route was being rearranged in order to put the ants into a test state, the exit tube from the nest was briefly blocked. The first section of channel was shortened from 7 m to 3 m for nest A and lengthened from 3 m to 7 m for nest B. The rest of the route was moved and reconnected to the shortened or lengthened channel (Fig. 1). The test route for nest A was thus equivalent to the training route of nest B, and vice versa. The exit from the nest was then opened and the exit from the feeder blocked.
Route C
To allow a faster changeover between training and testing, the arrangement
used for the third nest differed from the previous routes. In this arrangement
the first segment of the route from the nest comprised 5 m of channel made
from wooden walls embedded into the sand, with a rectangular cross-section 20
cm wide and walls 8.5 cm high. Tubing connected a further 1 m of plastic
channel continuing in the same direction as the wooden channel and leading
into a corner bucket. The first leg of the route was thus a total of 6 m. The
second leg of the route was another 2 m of the plastic channel leading at
right angles from the corner bucket to the feeder bucket with the same one-way
arrangement as in routes A and B.
To facilitate testing, we had a parallel test channel adjacent to the training channel, and removable doors in the nest closure so that ants could be funnelled into the appropriate channel. Instead of 5 m of the wooden sided channel, the test channel had 11 m of wooden channel before the configuration of buckets and plastic channels (1 m + 2 m). At first one channel was used for training and the other only for testing. Subsequently, the test channel was also shortened during training, so that the ants could then be switched between the two adjacent short (6 m + 2 m) channels every 2 h. The test channel was then lengthened before each test. The two methods gave similar results that have been pooled.
Recording and analysing home vectors
Ants taken at the feeders of all nests were tested in the same way. Each
ant was carried in a darkened vial from the feeder to the test area 100-400 m
away (depending on the nest). The test area was flat and featureless with a
grid of 1 m squares painted on to it. Each ant was released individually onto
the sand where there was a small sprinkling of biscuit crumbs, and the ant's
path over this grid was recorded on squared paper. Since ants perform more
reliable home vectors when carrying food, the ant's path was only recorded if
it picked up a crumb. To avoid interference from directional errors that ants
trained in channels tend to make in the middle of the day
(Müller, 1989), home
vectors were recorded either before 11:00 h or after 14:30 h. Ants were tested
no more than once a day and tests with the lengthened or shortened routes were
only every 2-3 days. Ants were trained for a minimum of 4 days before being
tested on an altered route.
The recorded trajectories from the release point to where the ant started
its search pattern (Wehner and Srinivasan,
1981) were digitised. The best-fitting line to a trajectory was
computed by the method of principal axes (see
Sokal and Rolf, 1995
, p. 586).
Circular statistics were used as prescribed by Batschelet
(1981
). The directions that are
given in the text are in terms of the absolute acute angle between the compass
direction of the segment of the L closest to the feeder and that of the
trajectory. Trajectory lengths were taken as the distance between the start of
the trajectory and the beginning of search behaviour
(Wehner and Srinivasan, 1981
).
95 or 99% confidence intervals (c.i.), gauged from fig. 5.2.2 in Batschelet
(1981
), were used to determine
whether the directions of mean trajectories differed significantly from
predictions.
To compare the trajectories of ants that were tested in different conditions, the endpoint of each trajectory was transformed into cartesian coordinates and a bivariate test (Hotellings T2) was used to decide whether the different conditions produced significantly different trajectories from the controls.
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Results |
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Home vectors from the shortened route A
Home vectors recorded when the first leg of route A was shortened from 8 m
to 4 m (mean direction 40.58±10.71°, N=20; mean length
3.95±1.30 m, N=20) reflect the parameters of the outward trip
that the ants have just taken and not the training parameters
(Fig. 2A). The endpoints of
shortened route A differed significantly from those of normal route A
(T2=58.87; F=28.939; d.f. 2,58;
P<0.001), but the shortened endpoints did not differ from those of
normal route B (T2=4.26; F=2.082; d.f. 2,42;
P=0.137). These data provide no evidence that ants recall a familiar
home vector when in a familiar location.
Home vectors from the lengthened route B
Fig. 2B shows the home
vectors for ants trained to route B (4 m + 4 m) and tested with the first leg
extended from 4 m to 8 m. The data were less clearcut than they were with the
previous route. When the first leg of the route was extended, the length of
the home vector (mean length 5.52±1.85 m, N=23) increased and
the direction (mean direction 57.80±10.09°, N=23) shifted
in the expected direction (62.5°) (Fig.
2B). The endpoints of the lengthened route B (8 m + 4 m) differed
significantly from the endpoints of the normal route B (4 m +4 m)
(T2=19.28; F=9.431; d.f. 2,45;
P<0.001) and did not differ significantly from the endpoints of
training route A (8 m + 4 m) (T2=4.557; F=2.24;
d.f. 2,61; P=0.115). Nonetheless, the changes were not as great as
one would have expected from the complementary data of
Fig. 2A. To try to understand
this result further, ants from this nest were retrained with the first leg
extended to 8 m. The length of the home vector then increased slightly (mean
length 6.24±1.81 m, N=29), but the direction (mean direction
56.17±9.62°, N=29) was essentially unchanged. The
endpoints of lengthened and retrained routes B were not significantly
different (T2=4.33; F=2.123; d.f. 2,49;
P=0.130) (Fig. 2B).
These data also provided no evidence that ants recall a familiar home vector
when in a familiar location.
Home vectors from route C
Because the results from route B did not appear straightforward when first
obtained, we decided to increase the difference between the training and test
conditions. Ants from a third nest were trained to a different L-shaped route
(6 m + 2 m) (Fig. 2C). As with
routes A and B, the mean direction of the global vector
(75.07±7.82°, N=27) corresponded closely to the predicted
direction of the nest from the feeder (69.6°). Also like routes A and B,
the mean length (5.3±1.66 m, 99% c.i. ±0.822 m, N=27)
was a little shorter (P<0.01) than the distance between feeder and
nest (6.6 m). In tests, the first leg of the route was extended from 6 m to 12
m. In this case, the direction of the vector rotated (83.37±12.67°,
N=31) to match the direction from feeder to nest (80.1°). The
home vector also increased in length (10.90±2.32 m, 99% c.i.
±1.073 m, N=31) but was again shorter (P<0.01)
than the distance between feeder and nest (12.4 m). The endpoints of the
training and lengthened routes differed significantly
(T2=164.93; F=80.996; d.f. 2, 55;
P<0.001). As in the results from nests A and B, the global home
vector after performing the lengthened foodward route corresponded to the
parameters of the altered route rather than to those of the training
route.
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Discussion |
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We have shown here, then, that ants do not discard a global PI state that conflicts with their previous experiences on the way to, or at, a familiar food site. When the beginning of a well-learnt route was lengthened or shortened, the ants' global homeward vector reflected the altered route rather than the habitual route. This finding complements the results of the previous studies mentioned in the Introduction, which show that also on the way back from a familiar food site, an ant does not discard a global PI state that disagrees with its previous experiences. Taken together, these studies suggest the general conclusions that, while desert ants may suppress guidance by global PI (for instance, by following local vectors or landmarks), they do not modify a global PI state that conflicts with their previous experiences. It is still possible that ants do possess a cumulative global PI memory of a food site, but its function would have to be to provide a target for the PI navigation system during the foodward trip, reflecting long-term experience of where abundant food is to be found, rather than to give a forager its current position. It appears that the current global PI coordinates of a foraging ant are set without the aid of landmarks or of cumulative memories, and are not modified by recognising a familiar location. The use of global PI on the return trip simply allows an ant to travel home after an outward trip that may differ from previous ones.
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Acknowledgments |
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