|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online December 14, 2005
Journal of Experimental Biology 209, 26-31 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.01976
Ant navigation: resetting the path integrator
Zoologisches Institut, Universitat Zurich, Winterthurestrasse 190, Zurich CH 8057, Switzerland
* Author for correspondence (e-mail: mknaden{at}zool.unizh.ch)
Accepted 9 November 2005
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Owing to its egocentric nature the path-integrator is error prone. Hence, it is a suitable strategy to reset the path integrator if the ant has appeared at its final goal, the nest. Otherwise during consecutive foraging runs navigational errors would steadily increase.
Key words: path integration, orientation, Cataglyphis fortis
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). Once they have completed their inbound (home) run and
arrived at the nest, their path integrator has again reached its zero state.
However, as Cataglyphis ants have been shown to be able to return to
an artificial feeder (e.g. Wehner,
1982) or to a natural feeding site
(Schmid-Hempel, 1983;
Wehner et al., 1983), along a
straight (outbound) path, the information about the path-integration vector is
not lost, but must reside in some kind of reference memory. Furthermore,
particular (open-jaw) training experiments show that Cataglyphis
never learns a feeder-directed (outbound) vector that is not the reverse of
the nest-directed (inbound) vector (for details see Collet et al., 1999;
Wehner et al., 2002).
Whatever the computational mechanism of the path integrator might be (for
models, see Mittelstaedt,
1983; Hartmann and Wehner,
1995; Collett and Collett,
2000), the results of previous experiments can conveniently be
described applying the following formalism (for conventions, see
Andel and Wehner, 2004). Let us
assume that the ants, having arrived at a feeding site, transfer the state of
their path integrator to some kind of reference memory (reference vector
R: R=+1 with the plus sign meaning R is pointing from the
feeder to the nest, and with the value 1 indicating the straight-line distance
between feeder and nest). Subsequently, while performing their homebound runs
the ants are considered to continually compare the current state C of
their path integrator (C=0 at the feeder) with the reference vector. If
C=+1, i.e. R-C=0, the ants have reached the nest. Before
setting out for a new foraging journey to the same feeding site, the ants
reverse the sign of their reference vector (R=-1 with the minus sign
meaning that R is pointing from the nest to the feeder) and walk until
R-C has again become zero. Then they should have arrived at the
feeding site.
The egocentric nature of the path-integration process makes it vulnerable
to the accumulation of errors. This problem gets larger the longer the
foraging journey lasts (Müller and
Wehner, 1988). The ants compensate for this error-proneness of the
path integrator by making additional use of route-defining and nest-defining
landmarks (Collett et al.,
1992; Wehner et al.,
1996; Bisch-Knaden and Wehner,
2003; for Australian desert ants Melophorus bagoti see
Kohler and Wehner, 2005).
In experiments designed to let the information provided by the path
integrator compete with information gained by familiar landmarks, the latter
is able to override the path integrator
(Sassi and Wehner, 1997), but
by itself does not reset it (Andel and
Wehner, 2004). For example, in one experiment
(Knaden and Wehner, 2005) the
entrance to a nest of Cataglyphis fortis was conspicuously marked by
an array of landmarks, a set of four large black cylinders positioned around
the nest entrance. After the ants had been trained to shuttle back and forth
between the feeder and the nest, they were displaced from the feeder to an
unfamiliar test area. Upon release they immediately set off in their prior
home direction and after having arrived at the vector-defined fictive position
of the nest (PV), started a systematic search for the
non-existing nest. At this time, the familiar nest-defining landmark array was
quickly installed some metres to the side of the fictive position of the nest.
The ants directly headed for the landmarks and searched narrowly at the
landmark-defined position (PL) of the (again non-existing)
nest. The question now was whether the search at the PL did
reset the path integrator such that the position of the nest would now be
defined by PL rather than by PV. The
answer was a clear no. After the landmarks were removed again, the ants did
not continue their search at PL, but switched back to
PV. Hence the landmarks had been clearly used by the ants as
stimuli defining the position of the nest (as the ants' intensive search there
had shown), but they had not been sufficient to reset the path integrator.
What cues are finally involved in the resetting process? This is the question
addressed in the present account.
|
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
In Experiment 1 we examined whether the immediate vicinity of the nest, with all its surrounding characteristics, be they visual or olfactory, suffices to reset the ant's path integrator. The ants were captured at the feeder and released directly at the nest entrance, i.e. less than 2 cm away from it. Untreated ants that moved from the nest to the feeder served as controls.
In Experiment 2, ants that had been trained in the same way as the ones in Experiment 1 were again captured at the feeder, but now forced to enter the nest. They were placed under an inverted jar on top of the nest entrance. The jar was removed after the experimental animals had disappeared into the nest. It took more than 2 min before this could be achieved and all ants had finally entered the nest. We then removed the feeder and recorded the ants' paths when they left the nest for the first time after they had been forced to enter it. In the following we will refer to these ants as `reset ants'. Again untreated ants that moved from the nest to the feeder served as controls.
Experiment 3
If in Experiments 1 and 2 the reset ants should actually head towards the
feeder, they could do so by relying on familiar landmarks or odour cues
present along their route from nest to feeder. In order to control for such
effects and to test whether any potential feeder-heading behaviour of outbound
ants was the result of information from the ant's path integrator, we designed
an experimental set-up that allowed us to exclude any external cues. A
circular wooden arena (1 m diameter, with a 5 cm grid marked on it) was placed
on top of a Cataglyphis nest (Fig.
1B). The natural nest entrance was connected with the centre of
the arena by a vertical metal pipe (diameter: 2 cm, length: 0.4 m), so that
all nest-leaving ants entered the arena through this pipe. The inner walls of
the pipe contained small twigs, so that the ants could easily ascend inside
the pipe. A brown plastic barrier (height: 3 cm) at the outer border of the
arena prevented the ants from escaping and excluded any view of landmarks. A
feeder trap filled with biscuit crumbs was installed by connecting a screw top
jar down under a hole (diameter: 1 cm, distance from nest: 0.48 m) in the
arena. During training, the ants were allowed to leave the feeder trap by a
paper ladder. Ants that had reached the feeder were individually marked by a
two-colour code. When one to three ants continuously shuttled back and forth
between nest and feeder, their runs to the feeder were recorded by a digital
camcorder. The position of the camcorder was changed continuously in order not
to be used as a landmark. We removed the paper ladder from the feeder and
waited until the focus ants were trapped inside the feeder jar. The whole
arena was turned by 180° in order to prevent the ants from using any arena
attached orientation guides (as there might have been odours or small optical
irregularities in the arena's ground or border). In order to prevent the ants
from using proprioceptive cues when leaving the nest, we also changed the
arrangement of the twigs within the pipe connecting the nest with the arena.
We then carefully poured the ants out of the feeder glass directly into the
metal pipe and video tracked the first emergence of the reset ants.
Experiment 4
Should the previous sets of experiments indeed show that the ants did reset
their path integrator once inside the nest, Experiment 4 should help us to
identify the nest-specific resetting cues. Ants that were trained and captured
as those in Experiments 1 and 2 were now put into small cages placed directly
into the nest entrance. These cages were small plastic tubes (diameter: 0.7
cm) with ends that were closed with metal mesh (mesh width: 0.8 mm). By
placing these cages into the nest entrance, the ants were able to antennate
with nestmates and to be exposed to possible nest-entrance specific odours (be
they volatile or attached to the walls of the nest entrance). A black cover
darkened the nest entrance and the cages. After 5 min the cover was removed
and the upper mesh was opened. As soon as the ants left the cages, we removed
the cages and recorded the trajectories of the ants as described above. Of
course, in this experiment the ants captured at the feeder and put into the
cages were not provided with food crumbs.
Data analysis
For Experiments 1, 2 and 4, we cut the trajectories at their first crossing
of a fictive 6-m circle around the nest entrance. The sinuosity of the runs
was computed by dividing the ant's path length by the bee-line distance
between nest and recording circle, i.e. by 6 m. Directionality (with
nest-to-feeder direction being defined as 0°) and sinuosity of the
experimental animals were compared with the corresponding data of the control
animals (circular statistics: Rayleigh test and Watson-Williams test; linear
statistics: Student's t-test).
In Experiment 3, the trajectories were cut at their first transgression of a 0.4 m circle around the nest entrance. An ant's last outbound run performed before the reset was taken as a control and its sinuosity and directionality were compared with those of the first run after the reset. As there are no tests available for paired circular data, we used the same circular statistics as above and the paired Student's t-test for the linear statistics.
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
|
Which are the nest-bound cues that reset the path integrator?
Having shown that cues inside the nest did reset the ant's path integrator,
we tried to specify these cues by conducting Experiment 4. The ants were
trained as in Experiments 1 and 2, and were again captured at the feeder, but
were now released into small cages positioned in the nest entrance hole that
allowed antennal contacts with the walls of the nest entrance and with
nestmates, for 5 min. Such contacts were in fact observed. After the cage had
been opened, the ants could have either followed their home vector (i.e. the
path integrator had not been reset by the ants' stay in the nest entrance), or
they could have moved directly into the nest (the path integrator had been
either reset or at least overridden by the nest cues), or they could have
headed directly towards the feeder (the path integrator had been reset, and
the feeder vector had been reloaded).
The ants behaved according to the first hypothesis. When they were allowed to leave the cage, only 4 out of 20 ants directly entered the nest, while 16 ants behaved as the ants had done in Experiment 1: they exhibited their home vector and ran for 7.2±2.2 m (N=16) towards the fictive nest (mean direction, 181°; N=16; r=0.917; Rayleigh test: P<0.001). Obviously, the intensive antennal contacts with nestmates and with the material of the entrance hole had not been sufficient for resetting the path integrator, even if the ants were exposed to this situation for 5 min in darkness, as is typical for the nest interior.
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Collett and Collett, 2000;
Wehner and Srinivasan, 2003).
In keeping with the formalism outlined in the Introduction, ants frequently
returning to the same feeding site acquire a reference vector R
pointing towards the feeder when the ants are at the nest and pointing at the
nest when the ants are at the feeder. They then move from either nest or
feeder until the current state C of their path integrator has reached
the state defined by the reference vector, i.e. until R-C=0.
What, however, happens when the ants have run off, say, their home vector,
i.e. when their path integrator is at zero state, but the nest has not been
reached yet, but is reached only later? In order to address this question we asked whether nest-bound cues were able to reset the path integrator even if R does not yet equal C.
As we expected from our previous work cues associated with the close vicinity of the nest did not suffice to reset the ant's path integrator. When ants were captured at the feeder and released close to the nest, they followed their still existing home vector (C=0) and departed from the nest (Fig. 2A). Actually, one of the 15 ants even stumbled into the entrance hole of the nest, but hurried out immediately and ran off its home vector.
However, when we changed the experimental paradigm just by the detail that
now the ants were forced to enter the nest entrance instead of being released
close to it, the result changed dramatically. In Experiment 2 all ants that
reappeared within 6 h at the nest entrance now headed towards the feeder, that
is, had turned their running direction by 180° compared to the one of
their former home vector (Fig.
2A). One could argue that in this time period the vector
information had decayed. This, however, is extremely unlikely as it has been
shown that vector information lasts for more than 2 days
(Ziegler and Wehner, 1997).
Repeating this experiment on a circular arena that was free from visual
landmarks confirmed that this directionality was the result of path
integration and not guided by any external cues
(Fig. 3). In terms of the model
described above, the ants had now reset their current vector C from 0
(feeder state) to 1 (nest state), while the reference vector R had
remained constant.
When the ants were transferred to dark cages and exposed there to nest odour and antennal contacts with nestmates, their path integrator was not reset. We, therefore, cannot yet define the decisive cues that cause the resetting process inside the nest.
In hamsters, Etienne et al.
(2004) showed that an episodic
view of a learned landmark array is able to reset the animal's path
integrator. As the hamster's path integration system is based completely on
idiothetic cues, path integration in hamsters is much more susceptible to
cumulative errors (Mittelstaedt and
Mittelstaedt, 1973; Benhamou et
al., 1990). In a similar experiment, Knaden and Wehner
(2005) exposed
Cataglyphis ants to a situation in which the position, at which the
ant's path integrator was at zero-state, did not coincide with the position of
the nest as marked by the familiar landmark panorama (see Introduction).
Contrary to what was observed in the hamsters, the landmarks did not suffice
for resetting the path integrator. This result again underlines the
predominant role path integration based on external (celestial) compass cues
plays in Cataglyphis. As our present data show, only cues bound to
the inside of the ants' colony are able to reset the path integrator.
What might be the ultimate reason for the reset of the path integrator inside the nest?
The egocentric nature of path integration results in a progressive
accumulation of errors when foraging journeys last too long
(Mittelstaedt and Mittelstaedt,
1973; Müller and Wehner,
1988; Wehner and Wehner,
1990). Because of these errors, at the end of the journey the
position of the nest, as defined by the path integrator, might not coincide
with the actual position of the nest. As long as the accumulated errors do not
become too large, the ants will at least reach the vicinity of the nest, where
they will then be guided home by the aid of nest-surrounding external cues.
However, when being guided to the nest by these cues, the path integrator is
still running (Andel and Wehner,
2004), so that when the ants finally enter the nest, the path
integrator is not at zero state anymore. Let us now assume that there would be
no reset occurring within the nest: as the reference vector pointing from the
nest towards the feeder is always the reverse of the reference vector pointing
from the feeder towards the nest (Collett
et al., 1999; Wehner et al.,
2002), the next foraging trip would not point exactly at the
feeder, but would be affected by the errors that had accumulated during the
ant's last inbound journey. Therefore, on consecutive foraging trips path
integration errors would steadily increase, and the information about the
nest-feeder (and feeder-nest) vector would increasingly deteriorate. Hence,
during a forager's lifetime repeated calibrations of the path integrator are
indispensable. As the nest provides an ant with specific and clearcut visual,
tactile, olfactory and social cues, it is certainly the best place at which
the path integrator could be reset reliably.
Dyer et al. (2002) describe
that when bees are captured at a feeder to which they have been trained before
and released there 3 h thereafter, their vanishing directions depended on the
filling state of their crops. With their crops filled the bees headed towards
the nest, whereas they headed in the direction opposite to the nest, when
their crops were only partially filled or empty. As to the latter group, Dyer
et al. (2002) suggested
"that the bees had determined that they were home and needed to fly
toward the food,...", i.e. that they had reset their current vector to
the nest state. This suggestion would imply that the bee actually being at the
feeder behaved as if it were at the nest. Rather, we prefer the alternative
hypothesis put forward by Wehner
(2003) that the bees having
not yet been completely successful at the feeder, and hence still being in
their foraging mode, would continue to venture out further in the former
foraging (nest-to-feeder) direction. This hypothesis is strongly supported by
the foraging strategy of Cataglyphis ants
(Wehner et al., 2004). Almost
every ant returned to a site from which they have retrieved a food item in the
immediately preceding foraging run. If next time they are unsuccessful there,
they continue their search in the former foraging direction. In terms of the
path integration concept mentioned above this means that the ant's path
integrator keeps running, i.e. the current vector C increases. Finally,
if the ant has found a food item at a new site, the state of the path
integrator defines a new reference vector R. In summary, the ant's path
integrator keeps running throughout. There is no need to assume that the
animal resets its path integrator to the nest state when it leaves the feeder
unsuccessfully. Furthermore, in a particularly well designed experimental
paradigm Andel and Wehner
(2004) showed that it is next
to impossible to reset the ant's path integrator, as long as the ant is
outside the nest.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Andel, D. and Wehner, R. (2004). Path integration in desert ants, Cataglyphis: how to make a homing ant run away from home. Proc. R. Soc. Lond. B 1547,1485 -1489.
Benhamou, S., Sauvé, J. P. and Bovet, P. (1990). Spatial memory in large-scale movements: efficiency and limitation of the egocentric coding process. J. Theor. Biol. 145,1 -12.
Bisch-Knaden, S. and Wehner, R. (2003). Landmark memories are more robust when acquired at the nest site than en route: experiments in desert ants. Naturwissenschaften 90,127 -130.[Medline]
Collett, M. and Collett, T. S. (2000). How do insects use path integration for their navigation? Biol. Cybern. 83,245 -259.[CrossRef][Medline]
Collett, M., Collett, T. S. and Wehner, R. (1999). Calibration of vector navigation in desert ants. Curr. Biol. 16,1031 -1034.
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.
Dyer, F. C., Gill, M. and Sharbowski, J. (2002). Motivation and vector navigation in honey bees. Naturwissenschaften 89,262 -264.[CrossRef][Medline]
Etienne, A. S., Maurer, R., Boulens, V., Levy, A. and Rowe,
T. (2004). Resetting the path integrator: a basic condition
for route-based navigation. J. Exp. Biol.
207,1491
-1508.
Hartmann, G. and Wehner, R. (1995). The ant's path integration system: a neural architecture. Biol. Cybern. 73,483 -497.
Knaden, M. and Wehner, R. (2005). Nest mark orientation in desert ants Cataglyphis: what does it do to the path integrator? Anim. Behav. doi:10.1016/j.anbehav.2005.03.030
Kohler, M. and Wehner, R. (2005). Idiosyncratic route-based memories in desert ants, Melophorus bagoti: How do they interact with path-integration vectors? Neurobiol. Learn. Mem. 83,1 -12.[CrossRef][Medline]
Mittelstaedt, H. (1983). The role of multimodel convergence in homing by path integration. Fortschr. Zool. 28,197 -212.
Mittelstaedt, H. and Mittelstaedt, M.-L. (1973). Mechanismen der Orientierung ohne richtende Aussenreize. Fortschr. Zool. 21,46 -58.
Müller, M. and Wehner, R. (1988). Path
integration in desert ants, Cataglyphis fortis. Proc.
Natl. Acad. Sci. USA 85,5287
-5290.
Sassi, S. and Wehner, R. (1997). Dead reckoning in desert ants, Cataglyphis fortis: can homeward-bound vectors be reactivated by familiar landmark configurations? Proc. Neurobiol. Conf. Göttingen 25,484 .
Schmid-Hempel, P. (1983). Foraging ecology and colony strtucture of two sympatric species of desert ants, Cataglyphis bicolor and Cataglyphis albicans. Dissertation, Universität Zürich.
Wehner, R. (1982). Himmelsnavigation bei Insekten. Neurophysiologie und Verhalten. Neujahrsblatt Naturforsch. Ges. Zürich 184,1 -132.
Wehner, R. (1992). Arthropods. In Animal Homing (ed. F. Papi), pp.45 -144. London: Chapman and Hall.
Wehner, R. (2003). Desert ant navigation: how miniature brains solve complex tasks. J. Comp. Physiol. A 189,579 -588.[CrossRef][Medline]
Wehner, R. and Srinivasan, M. V. (2003). Path integration in insects. In Biological Basis of Navigation (ed. K. Jeffery), pp. 9-30. Oxford: Oxford University Press.
Wehner, R. and Wehner, S. (1990). Insect navigation: use of maps or Ariadne's thread? Ethol. Ecol. Evol. 2,27 -48.
Wehner, R., Harkness, R. D. and Schmid-Hempel, P. (1983). Foraging strategies in individually searching ants, Cataglyphis bicolor (Hymenoptera, Formicidae). Stuttgart, New York: Fischer.
Wehner, R., Michel, B. and Antonsen, P. (1996). Visual navigation in insects: Coupling of egocentric and geocentric information. J. Exp. Biol. 199,129 -140.[Abstract]
Wehner, R., Gallizi, K., Frei, C. and Vesely, M. (2002). Calibration processes in desert ants navigation: vector courses and systematic search. J. Comp. Phys. A 188,683 -693.
Wehner, R., Meier, C. and Zollikofer, C. (2004). The ontogeny of foraging behaviour in desert ants, Cataglyphis bicolor. Ecol. Entomol. 29,240 -250.
Ziegler, P. E. and Wehner, R. (1997). Time-courses of memory decay in vector-based and landmark-based systems of navigation in desert ants Cataglyphis fortis. J. Comp. Physiol. A 181,13 -20.
This article has been cited by other articles:
|
|
 |
|
  A. Narendra, K. Cheng, and R. Wehner Acquiring, retaining and integrating memories of the outbound distance in the Australian desert ant Melophorus bagoti J. Exp. Biol., February 15, 2007; 210(4): 570 - 577. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
