|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online August 17, 2006
Journal of Experimental Biology 209, 3336-3344 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02364
Visual and tactile learning of ground structures in desert ants
University of Zurich, Institute of Zoology/Neurobiology, Winterthurerstrasse 190, 8057 Zurich, Switzerland
* Author for correspondence (e-mail: rwehner{at}zool.unizh.ch)
Accepted 5 June 2006
 |
Summary |
|---|
 TOP Summary IntroductionExperiment 1Experiment 2General discussionReferences |
|---|
Key words: Cataglyphis fortis, orientation, ground landmark, tactile learning
|
Introduction |
|---|
|
TOPSummaryIntroductionExperiment 1Experiment 2General discussionReferences |
|---|
; Collett and Collett,
2000; Wehner and Srinivasan,
2003; Wehner et al.,
2002). This mode of navigation relies on acquiring egocentric
information on the nest position by continuously integrating the path run by
the animal, and doing so by integrating directional information provided by
celestial cues and distance information provided, for example, by
proprioceptive cues. The outcome of this computational process enables the ant
to return to the nest without detour once an appropriate food item has been
found. However, due to the egocentric nature of the path integration process
the position of the nest entrance as defined by the path integrator (in the
following referred to as the PI-position) is subject to a continuous
accumulation of errors. In trying to eliminate this navigational uncertainty,
desert ants will, whenever possible, take advantage of landmark information,
in order to finally pinpoint the goal, the nest entrance, by recalling a
previously learnt panoramic image of the goal and comparing this reference
image with the current retinal image
(Wehner and Räber, 1979;
Cartwright and Collett, 1983;
Wehner et al., 1996;
Wehner, 2003). A basic setup
for testing the significance of landmark navigation with respect to path
integration consists in presenting the nestdefining landmarks in a position
(in the following referred to as the LM-position) that does not coincide with
the PI-position (e.g. Wehner et al.,
1996; Knaden and Wehner,
2005).
The landmarks used so far in this kind of cue competition experiment have
mostly been black cylindrical objects up to 50 cm high and 50 cm wide, i.e.
landmarks that have been several orders of magnitude larger than the animal
itself, but have mimicked the salt-bush vegetation at the borders of, and
sometimes within, the salt pans inhabited by Cataglyphis fortis
(Heusser and Wehner, 2001).
Owing to their sheer size, these landmarks could be recognized by the ants
from quite some distance. The area within which an animal can identify such
landmarks and use them for orientation is called the catchment area of the
landmark(s) in question (Cartwright and
Collett, 1983); hence, the larger the object, the wider its
catchment area.
In addition, there are already a few hints that ants can recognize minor
ground variations and use them during nest finding behaviour [Santschi,
fig. 4
(Santschi, 1913); Wehner
(Wehner, 1968), and R.W.,
unpublished observations]. Inspired by these episodic remarks we designed an
experimental setup that enabled us to test whether local variations in the
ground properties perceived by the ant's ventral retina can be learnt,
recognized and used as landmarks in a potentially similar way as
Cataglyphis fortis has been shown to use large, panoramic landmarks
that extend upwards from the ant's visual horizon. We further tested whether
ground structures can also be perceived by tactile rather than only by visual
means.
|
|
); flies (Seifert
and Heinzeller, 1989); spiders
(Albert et al., 2001). However,
apart from the moth, Manduca sexta, which uses mechanoreceptors on
its proboscis to locate nectar sources by exploiting tactile properties of
flower petals (Goyret and Raguso,
2006), there have been no studies published yet that demonstrate
the use of tactile cues in any navigational tasks. Hence in a second set of
experiments we focussed on the type of stimuli used by the ants in recognizing
the ground landmark. Again, the experiments were designed in such a way that
the LM-position and the PI-position were set into competition, but now the
test landmarks differed from the training landmarks either in their visual or
tactile properties. |
Experiment 1 |
|---|
|
TOPSummaryIntroductionExperiment 1Experiment 2General discussionReferences |
|---|
; Wehner et al.,
1996; Åkesson and Wehner,
2002; Bisch-Knaden and Wehner,
2003), and that has been set into competition with the ant's
path-integration system (Bregy and Wehner,
2003; Knaden and Wehner,
2005).
Materials and methods 1
All experiments (i.e. experiments 1 and 2) were performed with wild,
free-ranging salt-pan ants, Cataglyphis fortis
Forel 1902
(Wehner, 1983), at our
Maharès study site (southern Tunisia) during the months July to
September of the years 2004 and 2005.
Ants (nest coordinates: N43° 31.720', E010° 32.278') were trained to forage to a biscuit-crumb feeder located 9 m north of their nest. While foraging, the ants had to run back and forth between nest and feeder within a linear channel (height: 9 cm, width: 7 cm), with walls made of plywood boards and the base was natural salt-pan (Fig. 1), which they were not able to leave by themselves. During landmark training a piece of dark and very rough abrasive paper (1 m long, 7 cm wide) was placed on the ground of the channel as close to the nest entrance as possible (for detailed training situations see Table 1, column 3; Fig. 2). The foraging ants were forced to cross this piece of abrasive paper, and by this to experience optical and tactile cues that differed from the ones in the remainder of the channel. Furthermore the channel walls inhibited the ants from having a lateral view of the surroundings and thus prevented them from seeing additional natural landmarks potentially occurring in the vicinity of the experimental device.
|
|
Ants arriving at the feeder were marked with a day-specific colour code and
tested 1 or 2 days later. This training-and-test schedule ensured that the
ants had completed about 30 foraging round trips, before they were tested
(Åkesson and Wehner,
2002). In the critical tests the ants were captured at the feeder
and, while still carrying their food item, transferred to a separate test
channel (length: 18 m) running parallel to the training channel. The test
channel was free of foraging nest mates and food items. This procedure assured
that homebound ants searching for their nest could only rely on within-channel
landmarks or on their egocentric vector information. Depending on the
experimental paradigm the tested ants were confronted with an identical
reproduction of the ground landmark used during training, but presented at
varying positions relative to their point of release (tests 1A-E,
Table 1). Once the ants had run
off their home vector, they would start their systematic searches centred on
the point where they expected the nest to be
(Wehner and Srinivasan, 1981).
Within the linear test channel this kind of behaviour usually performed in
two-dimensional space is restricted to one dimension. Constrained by the
channel walls the back-and-forth running ants have to execute sharp turns of
direction (Sommer and Wehner,
2004). During this `linear search' six turning points were
recorded with a precision of 0.1 m. A turn was considered complete if the ant
continued to run in the new direction for at least 0.2 m. Each ant was tested
only once throughout the whole experiment. Tests in which the ants lost their
food item or left the test channel before completing the required number of
six turns or did not approach the landmark for 0.5 m were considered
unsuccessful and therefore excluded from the analysis.
Data analysis
As already mentioned an ant will change its behaviour after it has run off
its home vector in a straight path, and will search for the nest by systematic
back-and-forth movements centred on the fictive position of the nest entrance.
This behaviour allows us to calculate search density distributions. In order
to determine the search density distribution in each individual ant, we
divided the channel into virtual 0.1-m bins and calculated how often each bin
was visited by the ant. For normalization we then divided the number of visits
within each bin by the total number of visits within all bins.
Search densities of different test paradigms were compared to those of
control groups (`control 1' or `control 2'; for details, see
Table 1, column 7) by
Mann-Whitney U-tests (Mann and
Whitney, 1947). The analysis focussed on those sectors of the
compared data sets that included relevant points (`test area', see column 5 in
Table 1), e.g. the nest
position as defined by the landmark (LM-position) or the nest position as
defined by the ant's path integrator (PI-position).
Results 1
Do ants use ground landmarks?
The first set of experiments was aimed at determining whether
Cataglyphis ants, once transferred to the test channel, focussed
their nest search behaviour more sharply on the fictive position of the nest
if the ground landmark were present than if it were not. This was indeed the
case (Fig. 3). When ants were
trained with a landmark at the nest and confronted with the identical setup in
the test channel, i.e. with the LM-position coinciding with the PI-position
(Fig. 3: test 1A), the ants
searched mainly and consistently at the fictive position of the nest as
defined by both the landmark and the state of the path integrator. The height
and sharpness of the search peak significantly differed from that of ants that
had been trained and tested without any landmark
(Fig. 3: control 1) or that had
been trained with the landmark at the nest position, but had later been tested
without it (Fig. 3: control 2).
In fact, the ants' search behaviour did not significantly differ between both
types of control (Table 1, last
column, first row), but did so highly significantly between control 2 and test
1A (Table 1, last column, third
row). Hence, ground structures such as the ones used in the current set of
experiments are effectively used by the ants as signposts marking the nest
entrance.
|
Displaced ground landmarks and nest search
In the next set of experiments the ground landmark was set in competition
with the ant's path integrator. In technical terms, the LM-position and the
PI-position did not coincide. This was achieved by presenting the ants with
the landmark at a location at which they had not yet run off their home
vector, so that they had to decide between the PI-position and the LM-position
of their goal (Fig. 4). As a
control we used ants for which the landmarks present during training had been
removed in the test situation, so that they had to rely exclusively on their
path integrator (Fig. 4A,
control 2).
If the LM-position differed from the PI-position by 1.5 m (Fig. 4A: test 1B) the search density at the LM-position (7.5 m) was significantly higher than that at the corresponding position of the control animals. Actually, it was as high as the one obtained when the LM-position coincided with the PI-position (Fig. 4A: test 1A). If the LM-position was moved even closer to the ants' point of release, i.e. even further away from the PI-position (3 m; Fig. 4A: test 1C), the ants still focussed their search at the LM-position (6 m) more strongly than the control animals did (highly significant statistically). However, if the ants encountered their nest landmark very close to the point of their release, i.e. if the LM-position differed from the PI-position by 7 m (Fig. 4A: test 1D), the ants no longer used the landmark as an orientation cue. Their search density at the LM-position (3 m) did not differ from the corresponding one in the control 2. Mean values, standard deviations, and P values of all statistical tests mentioned in the paragraph above are given in the last three columns of Table 1.
|
|
Experiment 2 |
|---|
|
TOPSummaryIntroductionExperiment 1Experiment 2General discussionReferences |
|---|
Materials and methods 2
In the second set of experiments the ground landmark was altered stepwise
in both its optical and its tactile properties. All ants were trained with a
landmark that was black and rough, delivering high visual and tactile contrast
to the channel surroundings. Later, they were tested with landmarks differing
in their optical and tactile properties and having been displaced from the
PI-position towards the point of release of the ants, by 1.5 m (LM-position:
7.5 m; Fig. 7).
|
|
In analyzing the type of stimuli being used by the ants, in the test
situation different types of landmarks were applied (see
Table 2, columns 3 and 4 for
landmark description and Fig. 6
for their optical properties): a black and rough landmark identical to the
training landmark (test 2A); a landmark painted in the background colour of
the channel but identical in tactile cues with the training landmark (test
2B); and finally a blacksprayed piece of cardboard providing the same optic
but different tactile cues as the training landmark (test 2C). In a further
experiment we covered the lower hemispheres of the ants' eyes by applying
light-tight acrylic paint (after the ants had been trained) and put the ants
back into the nest (test 2D). Once the treated ants had reappeared at the
feeder, we provided them in the test situation with a grey and rough landmark.
Now the ants did not experience any visual cues-not even diffuse ones-that
could indicate the position of the ground structure
(Antonsen and Wehner, 1995).
After a successful test (see above) each ant was examined under a binocular
microscope to confirm that the coverage was still intact. As a result of this
post experimental test five of the 17 treated ants had to be excluded. In each
ant the search behaviour was recorded and the search density was computed by
following the same protocol as in experiment 1. The search density profiles of
the four experimental subgroups mentioned above were compared by applying the
Kruskal-Wallis test (Kruskal and Wallis,
1952) accompanied by the Dunn-Sidak Multiple Comparisons post test
(Hochberg and Tamhane,
1987).
|
Results 2
Relevant stimuli for ground landmark recognition
In the control experiment (test 2A), in which the optical and tactile
properties of the landmark coincided with the ones during training, the ants
searched consistently at the LM-position. However if either parameter of the
landmark was changed (optical properties: test 2B; tactile properties: test
2C), the ants behaved similarly to the ones in experiment 1 in which the ants
had never seen a landmark during training but were presented with one in the
test (Fig. 5: test 1E): they
avoided trespassing the altered landmark. This behaviour resulted in a clear
peak positioned directly in front of the landmark, far away from both the
LM-position and the PI-position (Fig.
7: tests 2B and 2C).
However, the search density distribution of the ants confronted with the invisible landmark (test 2B) was bimodal, exhibiting a second peak at the PI-position. If the ants had once happened to cross the landmark, they avoided the LM-position and searched at the PI-position. This bimodal distribution with maxima in front of the landmark and at the PI-position could also be observed if, prior to testing, the ants had been deprived of vision in their ventral field of view by covering the lower hemispheres of their eyes with light-tight paint (Fig. 7: test 2D). Even though the half-blind animals subsequently encountered a familiar tactile landmark, they nonetheless avoided trespassing it. The results of statistical tests are given in Table 2.
|
General discussion |
|---|
|
TOPSummaryIntroductionExperiment 1Experiment 2General discussionReferences |
|---|
;
Bregy and Wehner, 2003), small
ground structures are used as nest-defining landmarks only within certain
states of the ant's path-integration vector: if an ant has learnt a nest
landmark, later, during homing it expects this landmark to occur after it has
fully run off its home vector. But as all vector navigation is error prone,
landmarks of any kind will help in finally pinpointing the goal. Particularly,
ants might accept a landmark at different states of their home vector, i.e.
even though they have not yet completed their vector-based home run. In the
present study, the ground landmark was accepted by the ant as a nest-defining
orientation cue at vector states of 100%, 83% and 66%
(Table 1: tests 1A-1C), but it
was ignored at the 22% state (Table
1: test 1D). This result is very similar indeed, even in
quantitative terms, with the results obtained by using large panoramic
landmarks as nest defining cues (Bregy and
Wehner, 2003).
However, the influence a familiar ground landmark has on the ant's search
pattern is limited: the centre of search cannot be shifted by the ground
landmark as drastically away from a position defined by the ant's path
integrator as is the case with panoramic landmarks (e.g.
Knaden and Wehner, 2005). This
can easily be explained by the reduced catchment area of ground marks. Whereas
large panoramic landmarks can be seen from far away, a ground landmark can be
recognized by the ant's ventral field of view and by the mechanoreceptors of
the ant's tarsi only if the ant is directly above it. If the ant leaves the
structure and loses it not only tactilely, but also visually, it instead
continues to rely on its path-integration vector. Knaden and Wehner
(Knaden and Wehner, 2005) have
shown a similar effect with panoramic visual landmarks. If in the test field a
set of nest-defining cylindrical landmarks was placed at a position that
differed from the position defined by the ant's path integrator, i.e. if the
LM-position and PI-position did not coincide, the ants first searched,
unsuccessfully of course, at the PI-position and -after the landmarks had been
installed-switched to the LM-position, but after removal of the landmarks by
the experimenter, returned immediately to the PI-position. This shows that the
path integrator keeps running all the time, even if the ants happen to rely,
at a particular instance, on landmark information.
|
The importance of the tactile properties of a ground landmark could be shown most directly in the experiments in which the ventral halves of the ant's eyes were covered with light-tight paint, so that any visual input from the ground structure was abolished. Yet the ants, if forced to perform their home run in the test channel, avoided a novel ground mark. Hence mechanosensory information alone suffices in detecting ground structures. But visual information alone does so as well. In fact, whenever in the test situation the ground landmarks were changed relative to the training situation in either their optical or their tactile properties, the ants exhibited an avoidance response (Fig. 7: tests 2B and 2C). Obviously, in either case the landmarks were no longer recognized as the ones with which the ants had been familiar in the training situation.
But how exactly did the animals perceive the tactile information provided
by the ground structures offered in the present case? The structures used in
this study most obviously differed in surface roughness, i.e. in the height
and the frequency of the deposited grains. As a qualitative analysis of
numerous high-speed video recordings (e.g.
Seidl et al., 2004) did not
provide any hint that the ants used their antennae for evaluating surface
structures during locomotion, the tarsi are the most probable appendages for
analysing the geometric surface properties. If we compare the geometry of an
ant's tarsi with the surface profiles of the ground structures used in this
study (Fig. 9), we find that on
the sanded channel ground the ant's tarsi would come to lie on top of a layer
of densely deposited grains, whereas in the case of the abrasive paper they
would fit in between the gaps of the loosely spread substructures of the
paper. Tactile hairs on the tarsi could determine the geometry of the surface
structure by monitoring both grain height and deposition frequency. Another
possible way for the ants to monitor surface structures would be to exploit
surface elasticity by, e.g. campaniform sensilla within the cuticle or
muscular strain sensors during touch down or lift off of the tarsi. Even
though mechanoreception is a well known sensory capacity in insects (e.g.
Römer, 2003), most
studies deal with mechanoreceptors located at the antennae (e.g.
Martin and Lindauer, 1966).
Tarsal mechanoreceptors have so far been studied in spiders (e.g.
Foelix, 1970), but not yet in
insects.
|
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionExperiment 1Experiment 2General discussionReferences |
|---|
Åkesson, S. and Wehner, R. (2002). Visual
navigation in desert ants Cataglyphis fortis: are snapshots coupled
to a celestial system of reference? J. Exp. Biol.
205,1971
-1978.
Albert, J. T., Friedrich, O. C., Dechant, H.-E. and Barth, F. G. (2001). Arthropod touch reception: spider hair sensilla as rapid touch detectors. J. Comp. Physiol. A 187,303 -312.[Medline]
Antonsen, P. and Wehner, R. (1995). Visual field topology of the desert ant's snapshot. Proc. Neurobiol. Conf. Göttingen 23,42 .
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]
Bregy, P. and Wehner, R. (2003). Beacon versus vector navigation in homing ants, Cataglyphis fortis. Neurobiol. Conf. 29,574 .
Cartwright, B. A. and Collett, T. S. (1983). Landmark learning in bees: experiments and models. J. Comp. Physiol. A 151,521 -543.[CrossRef]
Collett, M. and Collett, T. S. (2000). How do insects use path integration for their navigation? Biol. Cybern. 83,245 -259.[CrossRef][Medline]
Foelix, R. (1970). Structure and function of tarsal sensilla in the spider Araneus diadematus. J. Exp. Zool. 175,99 -124.[CrossRef]
Forel, A. (1902). Les fourmis du Sahara algérien. Ann. Soc. Entomol. Belgique46,147 -158.
Gnatzy, W. and Hustert, R. (1989). Mechanoreceptors in behaviour. In Cricket Behaviour and Neurobiology (ed. F. Huber, T. E. Moore and W. Loher), pp.198 -226. Ithaca, London: Cornell University Press.
Goyret, J. and Raguso, R. A. (2006). The role
of mechanosensory input in flower handling efficiency and learning by
Manduca sexta. J. Exp. Biol.
209,1585
-1593.
Heusser, D. and Wehner, R. (2001). The visual centring response in desert ants, Cataglyphis fortis. J. Exp. Biol. 205,585 -590.
Hochberg, Y. and Tamhane, A. C. (1987). Multiple Comparison Procedures. New York: Wiley.
Knaden, M. and Wehner, R. (2005). Nest mark orientation in desert ants Cataglyphis: what does it do to the path integrator? Anim. Behav. 70,1349 -1354.[CrossRef]
Kollmeier, T. (2005). Spektrale Kontrastanalyse zur beleuchtungsinvarianten Detektion von Landmarken. Diploma thesis, University of Bielefeld, Germany.
Kruskal, W. H. and Wallis, W. A. (1952). Use of ranks in one-criterion variance analysis. J. Am. Stat. Assoc. 47,583 -621.[CrossRef]
Mann, H. B. and Whitney, D. R. (1947). On a test whether one of two random variables is stochastically larger than the other. Ann. Math. Stat. 18, 50-60.
Martin, H. and Lindauer, M. (1966). Sinnesphysiologische Leistungen beim Wabenbau der Honigbiene. Z. Vergl. Physiol. 53,372 -404.[CrossRef]
Römer, H. (2003). Mechanorezeption. In Lehrbuch der Entomologie (ed. K. Dettner and W. Peters), pp. 281-298. Heidelberg, Berlin: Spektrum.
Santschi, F. (1913). Comment s'orientent les fourmis. Rev. Suisse Zool. 21,347 -425.
Seidl, T., Weihmann, T., Blickhan, R. and Wehner, R. (2004). Kinematic analysis of ants running at different inclinations. Comp. Biochem. Physiol. 137A,S102 -S103.
Seifert, P. and Heinzeller, T. (1989). Mechanical, sensory and glandular structures in the tarsal unguitractor apparatus of Chironomus riparius (Diptera, Chironomidae). Zoomorphology 109,71 -78.[CrossRef]
Sommer, S. and Wehner, R. (2004). The ant's estimation of distance travelled: experiments with desert ants, Cataglyphis fortis. J. Comp. Physiol. A 190, 1-6.[CrossRef][Medline]
Wehner, R. (1968). Optische Orientierungsmechanismen im Heimkehrverhalten von Cataglyphis bicolor (Formicidae, Hymenoptera). Rev. Suisse Zool. 75,1076 -1085.
Wehner, R. (1983). Taxonomie, Funktionsmorphologie und Zoogeographie der saharischen Wüstenameise Cataglyphis fortis (Forel 1902) stat. nov. (Insecta: Hymenoptera: Formicidae). Senckenb. Biol. 64, 89-132.
Wehner, R. (1992). Arthropods. In Animal Homing (ed. F. Papi), pp.45 -144. London: Chapman & 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 Räber, F. (1979). Visual spatial memory in desert ants, Cataglyphis bicolor (Hymenoptera: Formicidae). Experientia 35,1569 -1571.[CrossRef]
Wehner, R. and Srinivasan, M. V. (1981), Searching behaviour of desert ants, genus Cataglyphis (Formicidae, Hymenoptera). J. Comp. Physiol. A 142,315 -338.[CrossRef]
Wehner, R. and Srinivasan, M. V. (2003). Path integration in insects. In The Neurobiology of Spatial Behaviour (ed. K. J. Jeffery), pp. 9-30. Oxford: Oxford University Press.
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., Gallizzi, K., Frei, C. and Vesely, M. (2002). Calibration processes in desert ant navigation: vector courses and systematic search. J. Comp. Physiol. A 188,683 -693.[CrossRef][Medline]
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
