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First published online January 17, 2007
Journal of Experimental Biology 210, 375-382 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02674
Hair plate mechanoreceptors associated with body segments are not necessary for three-dimensional path integration in desert ants, Cataglyphis fortis
1 Department of Neurobiology, University of Ulm, Albert-Einstein-Allee 11,
D-89069 Ulm, Germany
2 Institute of Zoology, University of Zürich, Winterthurerstrasse 190,
CH-8057 Zürich, Switzerland
* Author for correspondence (e-mail: matthias.wittlinger{at}gmx.de)
Accepted 28 November 2006
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Key words: desert ant, Cataglyphis, navigation, 3-D path integrator, graviception
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Müller and Wehner,
1988), as a major means of orientation when foraging in their
typically flat and featureless desert habitat. Path integration relies on two
input components. The first is the direction of travel, measured by a
celestial compass. This compass is sensitive to the polarisation pattern of
sky light, to the sun's azimuth and to spectral gradients of sky light
(Wehner, 1992). The second
component for path integration is distance measurement, provided by an
odometer module. The ant odometer is basically a stride integrator that also
considers stride length or stride frequency
(Wittlinger et al., 2006;
Wittlinger et al., 2007).
Path integration in desert ants is surprisingly accurate and successful,
due to a number of compensatory and backup mechanisms that deal with the
inevitable navigation errors inherent in all integration mechanisms
(Müller and Wehner, 1988).
This accuracy is not too surprising for the compass module, which relies on
exact external directional cues, namely sun azimuth and sky light pattern. The
odometer module, by contrast, has to rely primarily on idiothetic cues, namely
proprioceptive signals that measure leg movement or monitor the output of a
locomotor central pattern generator
(Wehner, 1992;
Wittlinger et al., 2007). It
might thus be expected to be more error-prone than the directional component
of the path integrator. All the more surprising are unexpected features of the
odometer module that have been reported in recent years. Most notably, the
odometer is able to determine travel distance not just in the typical flat
desert pans but also in hilly terrain with slope inclinations of up to 60°
(Wohlgemuth et al., 2001;
Wohlgemuth et al., 2002;
Grah et al., 2005). Ants
walking over such hilly terrain determine the ground, or base line, distance
irrespective of the actual shape of the surmounted hills. This allows accurate
return to the nest on a different route from that taken during outbound
travel, independent of the substrate structure on these routes. Not only is
this feature of the ant odometer surprising but also its accuracy is
comparable to that achieved on level ground.
It is as yet completely unclear how base line distance is determined by the
ants when walking on hilly terrain. It is clear, however, that the ants must
be able to measure the slope of their walking substrate quite exactly to
achieve this feat. In the present study, we examine one particular hypothesis
of how desert ants might be able to determine the inclination of the ground
they travel on. According to the detailed analyses of Markl, ants determine
the relative positions of their body parts, such as head, thorax (or in ants,
alitrunk) and abdomen (or in ants, gaster), by means of hair fields associated
with the joints between these body segments
(Markl, 1962). And since the
pull of gravity on these segments is dependent on body position and
inclination, these hair fields might indeed serve as graviceptors involved in
adjusting the odometer module to substrate inclination.
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Materials and methods |
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) were selected.
The experimental seasons lasted from the middle of June to the start of
September in the years 2004 and 2005.
Preparation
To manipulate graviception, in a first set of experiments (exp. data I) the
hair sensillae in the neck region and/or those associated with the petiole
were eliminated by shaving with a razor splinter. There are two groups of hair
plates associated with the petiole, one between alitrunk and petiole and a
second between petiole and gaster (Fig.
1). In a second set of experiments (exp. data II), the joints
between head and alitrunk and those between alitrunk and gaster were
immobilised with a beeswax–resin mixture (1:2 v/v). In detail, the head
was fixed to the alitrunk in a normal attitude, while the gaster was fixed to
the alitrunk either in an extended position (i.e. gaster, petiole and alitrunk
forming a roughly straight line, 180°) or in an erect position (the angle
between alitrunk and gaster was <90°)
(Fig. 2).
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;
Wohlgemuth et al., 2002). Ants
were trained to forage at a feeder they could reach only via a series
of artificial hills (hill training) (Fig.
3), affording a walking distance of 10 m. That walking distance
corresponded to a distance on ground level between nest entrance and feeder of
6 m. As a control, a group of ants was trained to walk a 10 m distance in a
flat channel (flat training) (Fig.
3). For testing, the experimental ants were put into a horizontal
channel, 21 m long and oriented in parallel to the outbound (hill or flat
training) channel (Fig. 3)
(test). Both the artificial hill channel set-up for training (10 symmetrical
triangular `hills', consisting of 50 cm ascent and 50 cm descent, each with
slopes of 54°) and the flat channel set-up for control training and
testing consisted of alloy U-profiles. Width and height of the channels were 7
cm (see Fig. 3, top left), such
that the ants experienced a strip-like view of the sky of approximately
54° when walking in the centre of the channel profile (centring response)
(Heusser and Wehner, 2002) to
read the skylight pattern. To provide traction for walking, the channel floor
was coated with grey quartz sand, and to reduce optic movement cues and avoid
distracting reflections the walls were painted with matt grey varnish.
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) and performed
determined homebound runs. This experimental group performed the outbound
travel in a normal condition (`0'), and the homebound travel in a manipulated
condition (`1'), and is thus termed `0–1' throughout the text. After
this first test, the ants were released into their nest. A further (control)
test was performed in these manipulated ants after they had re-emerged from
the nest and performed another journey to the feeder (outbound manipulated
– homebound manipulated; `1–1' ants). In animals with immobilised
body segments (head–alitrunk or alitrunk–petiole–gaster
joints incapacitated), additional tests were carried out. Namely, one test was
made after removal of the beeswax–resin glue at the feeding site, thus
making the previously immobilised body parts again free to move (outbound
manipulated – homebound normal; `1–0'), and one final control test
was made after these 1–0 animals had reemerged from the nest, being in a
normal condition again (outbound normal – homebound normal; 0–0a;
as opposed to 0–0, as the group of ants tested prior to any
manipulation, except colour marking). Of course, the shaving of hair plates
could not be reverted in this way, the final test for these animals being
1–1.
Once transferred into the (flat) test channel, the ants performed their homebound runs. We recorded the point at which the ants switched from their steady, straight return path to their typical nest-searching behaviour. This point is marked by a conspicuous U-turn, followed by a run pacing back and forth around the initial turning point. The median distances of the six initial U-turns, relative to the release point, and the search densities were evaluated (see Figs 4, 5, 6). The test channel was divided into 10 cm bins for distance recording. Search density distributions (Figs 4, 5, 6, upper panels) were evaluated for each experimental situation. The bins of the test channel covered by an ant during its search were noted and cumulated, i.e. the more often a channel segment (bin) was visited during the search, the higher its value in the density distribution. Search density distributions were normalised to their peak values.
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Statistical tests
For descriptive statistics, box and whisker plots (box plots) are shown
(see Figs 4,
5,
6, lower panels). They display
median values (bar in the box) and interquartile ranges (IQR) as measures of
statistical dispersion, with first and third quartiles (the box margins) and
the 5th and 95th percentiles (whisker margins). For all tests, we performed
non-parametric statistics. Friedman Repeated-Measures ANOVA on Ranks compared
effects of a series of different experimental test situations on a single
group. If a difference was found, Tukey's test was performed as post
hoc-test for multiple comparisons between test situations
(Sachs, 1992). All statistical
analyses were made with SigmaStat Version 2.03 (SPSS Inc., Chicago, IL,
USA).
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),
control animals without any manipulation exhibited homing distances close to
the actual ground distance of the training set-up (0–0 in
Fig. 3A–C). In
experimental animals, the hair plates between head, alitrunk and gaster were
manipulated by shaving the hair sensillae in a first set of experiments.
Unexpectedly, none of the shaving operations changed the animals' homing
distances and, in particular, they did not extend them towards the 10 m actual
walking distance experienced during the outbound journeys
(Fig. 4). If anything, the ants
slightly underestimated, rather than overestimated, the distance to the nest.
This held true for all combinations of hair plate manipulation, shaving of the
hair sensillae in the neck region, of the hair plates associated with petiole
and gaster, and shaving of all these sets of hair plates (summary in
Table 1). The slight
underestimation of homing distance just noted was statistically significant
only for the animals that had all these hair sensillae incapacitated and were
tested after they had accomplished their first manipulated homing run
(1–1 animals, P<0.05, Tukey test)
(Fig. 4C).
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Shaving of hair fields – flat channel training controls
In these control experiments, the ants were trained from the nest entrance
to the feeder over a 10 m distance in a flat, linear channel, instead of the
artificial hill array used otherwise. The ants were tested in the usual 21 m
long flat channel. Interestingly, the slight underestimation of homing
distance after the shaving operations also occurred with the flat channel
training array (Fig. 5A,B).
Actually, animals that re-emerged from the nest after having previously been
shaved in the neck region (1–1) significantly (P<0.5, Tukey
test) undershot in their homebound runs, compared with the control recordings
in these same animals (0–0). Animals with their hair sensillae shaved in
the petiole–gaster region showed a significant underestimation of their
homing distance, compared with the control situation (0–0), in both
tests that followed the manipulation (0–1 and 1–1, both
P<0.5, Tukey test). These slight underestimations of travel
distance correspond to those observed with training in the artificial hill
array.
Immobilising body parts
There are two major differences between the shaving of hair plates and the
immobilisation of body segments. First, the hair plates associated with
immobilised body parts will constantly signal the particular fixed body
posture, while signalling is absent or corresponds to a `null' position after
shaving. Second, the immobilisation of body parts – here,
head–alitrunk and alitrunk–petiole–gaster joints – is
reversible. This expanded the test runs to be performed for any given ant by
another two runs: outbound journey, manipulated – homebound journey,
normal (1–0), and outbound journey, normal – homebound journey,
normal (0–0a) (in addition to the usual 0–1 and 1–1 tests).
That is, the animals were tested right after removal of the
beeswax–resin glue at the feeding site (1–0) and later, after they
had once again re-emerged from the nest and travelled to the feeder
(0–0a).
Unfortunately, ants with their head fixed to the alitrunk could not be
tested right after this manipulation, even when care was taken to adjust the
head in a fairly normal posture. They were confused, had problems cleaning
their antennae with the comb on their front legs and thus refused to accept a
food crumb. Carrying food in their mandibles, however, is evidence of the
ants' normal motivation to carry their booty home
(Wehner, 1982) and was thus a
prerequisite for recording homing distances (see Materials and methods).
Nevertheless, the operated animals appeared one day later from the nest with
their heads still immobilised, now apparently without problems, and travelled
to the feeder. The 1–1 test series could thus be performed, although
without the normal preceding 0–1 test run. No differences were observed
in the homing distances between these tests and the subsequent 1–0 and
0–0a tests (Fig. 6B). In
all these tests, the ants appeared to slightly underestimate ground distance,
instead of overestimating it due to the much longer outbound walking distance
of 10 m across the artificial hills array (see above).
Animals that had their gaster fixed in an extended position (180°) were tested immediately after the gaster had been glued to the alitrunk at the feeder. These ants, too, slightly underestimated their homeward travel distance on level ground. In the subsequent tests (1–1, 1–0, 0–0a), they searched even closer to the release point than right after the manipulation (0–1) (differences significant in 1–0 and 0–0a, compared with 0–1, P<0.05, Tukey test). The search density distributions in Fig. 6A (upper panel) demonstrate that this undershoot was quite distinct, the distribution of test 0–1, by comparison, showing a consistent shift towards larger distances.
The most striking results were observed in ants that had their gaster fixed in an erect position (<90°). Ants that had their gaster immobilised during outbound as well as homebound runs (1–1) significantly underestimated homing distances, both after training in the horizontal channel and in the artificial hill array (P<0.05, Tukey test) (see Fig. 6C, Fig. 5C). Very distinct displacements of the search density distributions towards the shorter homing distances were observed in these experiments (Fig. 6C, Fig. 5C, upper panels). This held true to some extent even after removal of the immobilising glue before the animals started their homebound journey (1–0) (see Fig. 6C). This pronounced underestimation in the 1–1 and 1–0 tests of the artificial hill training and in the 1–1 tests of the flat channel training were conspicuous indeed, particularly when considering the rather consistent results of all the other experiments.
The above results are summarised in Table 1.
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), ants foraging in
the artificial hill channel array would have no perception of the surmounted
up- and downward slopes. They should thus perform homebound journeys in the
flat test channel that correspond to the actual walking distance of 10 m of
their outbound journey in the artificial hill array (in the critical 1–1
tests). At the very least, one would expect the animals to extend their search
for the nest entrance well beyond the base line distance of 6 m. In contrast
to this expectation, the experimental animals consistently performed homebound
journeys that corresponded to the ground level distance of their outbound
journeys. In several instances, the ants actually searched for the nest
entrance at even shorter distances from the release point. This was true for
both experimental interferences, i.e. shaving of the hair fields and
immobilisation of the body parts monitored by these position sensors
(summarised in Table 1). These
results demonstrate that manipulated animals were still able to perform
(almost) correct path integration during their up- and downhill outbound
journeys.
This result is surprising when considering, first, that
Cataglyphis ants usually keep their gaster in an upward (erect)
position (see Fig. 2A) and,
second, that, due to their long legs and elevated centre of mass, the gaster
would lend itself as a major means of detecting terrain slope. More
significantly, in his careful behavioural study of graviception in formicine
ants, Markl identified the hair sensillae in the neck and petiole regions as
important sensors for graviception (Markl,
1962).
In the above experiments, the hair plates associated with the legs and
antennae still remain as possible sensors of the slopes of ascent and descent
during outbound travel. Unfortunately, the hair fields of coxa and trochanter
are not accessible for operation or immobilisation, at least not without
incapacitating the animals and thus preventing further homing experiments.
Operating the antennae has similarly severe effects. However, Markl suggests
that the neck joint and the alitrunk–petiole–gaster joints are of
particular importance for graviception and slope detection
(Markl, 1962). At the very
least, the relative contributions to graviception of these hair plates and
those associated with the legs are in the same order of magnitude and cannot
completely replace each other. Thus, the hair plates remaining on the legs
would not appear to be responsible for the largely unaffected path integration
in uneven terrain. Wohlgemuth and co-workers demonstrated, in an experimental
set-up similar to the one used here, that additional loads applied on the
alitrunk did not induce misjudgement of base line distance
(Wohlgemuth et al., 2002).
Presumably, thus, hill slopes were also judged correctly. The authors conclude
that the artificial load could only have affected the legs, and thus the hair
sensillae associated with the joints between leg segments, but could not have
impaired other body parts such as head, petiole and gaster. Hence, the
detection of slopes must have remained unaffected with altered leg load and
slightly changed leg coordination.
In summary, it appears that desert ants do not measure terrain slope by means of sensory systems employed in graviception, namely neither by hair fields associated with neck and petiole nor by those associated with the legs. At least, these organs are dispensable for 3-D path integration and their loss can be compensated. It remains to be examined whether the ants use different sensory modalities altogether, such as vision and the detection of sky light polarisation, to assess the slope of their walking substrate.
Possible reasons for underestimation of homing distance
Apparent underestimation of homing distance was observed in several of our
experiments (see e.g. Figs 4,
6; summarised in
Table 1). Modest undershoot may
in fact represent an element of homing strategy, rather than a genuine mistake
in distance estimation. Starting to search for the nest after a homing
distance that is shorter than the actual estimate by the average margin of
error will lead the animal to the familiar side of the nest surrounds, rather
than to unfamiliar terrain beyond the nest (see also
Sommer and Wehner, 2004;
Wolf and Wehner, 2005). Such
undershoot in the range of about 5–10% of homing distance is thus
frequently observed in homing experiments, not only in desert ants (see
Sommer and Wehner, 2004). This
effect may become more pronounced in cases where the animals experience
disturbances or are even disabled. In such cases, it may be advantageous to
opt for more safety at the expense of homing speed. According to this line of
argument, a more severely impaired ant should exhibit shorter homing
distances, at least within the short-distance ranges examined here (6–10
m, compared with more than 100 m in some recorded foraging runs; for these
distances this argument may not be valid any more).
Gluing the gaster to the alitrunk in an (extremely) erect position
(<90°) had the most noticeable effects on homing distance, both in the
up- and downhill channel training and in the flat channel training
(Fig. 5C,
Fig. 6C). In these experiments,
the undershoot was pronounced to an extent that makes the above general
explanation for shortened homing distances very unlikely. At the same time,
this manipulation had the largest impact on body posture, since the position
of an ant's centre of mass is noticeably influenced by fixing the heavy gaster
onto the alitrunk (see Fig. 2D)
(Zollikofer, 1988). In the
artificial hill training, these animals considerably underestimated their
travel distance, by an average 75.6%, when tested after they had emerged with
their fixed gaster at the feeding site (1–1). This held true when the
manipulation was reversed at the feeder and the animals were tested again,
although the undershoot was somewhat smaller (50%) (1–0)
(Fig. 6C). Intriguingly, the
ants also misgauged their travel distance in the flat channel (control)
experiment, though only when the gaster was fixed during both outbound and
homebound runs (1–1). They did not undershoot when the manipulation was
reversed before the homebound run was performed (1–0)
(Fig. 5C).
Outbound journey with the gaster fixed in an extreme erect position thus seems to be the major determinant in misgauging homing distance in these experiments. At present, one can only speculate about the possible reasons for these observations.
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Acknowledgments |
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180°) position. (B) Animals with their head fixed in a normal
position. (C) Animals with their gaster fixed in an erect (<90°)
position.