Desert ants compensate for navigation uncertainty
1 Department of Neurobiology, University of Ulm, D-89069 Ulm,
Germany
2 Institute of Zoology, University of Zurich, CH-8057 Zurich,
Switzerland
* Author for correspondence (e-mail: harald.wolf{at}uni-ulm.de)
Accepted 28 September 2005
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
This approach behaviour was examined in more detail in order to identify the underlying orientation strategy. First, the ants may employ a `goal expansion strategy', using odour spread as a spatially limited indicator for the presence of food. In that case, the distance steered downwind of the feeder should be determined by the range of the odour plume (and, for instance, wind speed). It should be independent of the distance between nest and feeder. Second, the ants may apply an `error compensation strategy', using odour filaments as a guideline towards the food source. Steering downwind by a margin just exceeding their maximum navigation error will lead the ants safely across the odour guide. In that case, the distance steered downwind of the feeder should increase more or less linearly with the nest-feeder distance.
Our results unambiguously support the second strategy. When feeders were established at distances of 5-75 m from the nest, the distances steered downwind of the food increased from 0.7 m to 3.4 m in a linear fashion. This result was independent of wind speed or wind direction. It translates into an ant's estimate of its navigation error within a range of 3° to 8°.
Key words: insect, Cataglyphis fortis, navigation, uncertainty, error compensation
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
A second strategy was used by Polynesians until recent times. In the vast Pacific Ocean, small islands were difficult to locate to within eyeshot without extensive searching. Navigators relied on secondary long-range indicators of the presence of land, for instance, wave patterns, clouds or sea bird behaviour. This `goal expansion strategy' restricted the search space considerably and reduced the effort to find small islands. It is unknown whether or not animals employ similar strategies to deal with navigation errors.
Desert ants, Cataglyphis fortis, achieve remarkable orientation
feats. Foraging trips may lead a worker ant more than 100 m - or roughly 10
000 times its body length - away from the nest entrance. Upon encountering a
prey item, the ant returns to the inconspicuous nest entrance on an almost
straight path, relying exclusively on its path integration system, as its salt
pan habitat is almost devoid of landmarks (for reviews see Wehner,
1992,
1996
). Despite such impressive
orientation performance, navigation errors may prevent the animals from
directly encountering their nest entrance, which is often just a couple of
centimetres in diameter. Desert ants possess a number of strategies to deal
with these navigation errors and other uncertainties. For example, if they
miss their nest entrance upon returning from a foraging trip, they perform a
systematic search centred on the assumed location of the nest entrance
(Müller and Wehner, 1994
).
The ants also employ their path integration system for relocating previously
visited places, in particular, reliable food sources (e.g.
Wolf and Wehner, 2000
).
However, when visiting a familiar food source, the ants do not only rely on
path integration but also use olfactory and anemotactic cues
(Wolf and Wehner, 2000
; see
also Linsenmair, 1973
). When a
constant wind is blowing, as is characteristic of their desert habitat, the
ants do not approach the feeder directly. Rather, they steer some distance
downwind of the food source, and when they pick up the odour filaments
emanating from the food, they follow this odour trail upwind towards the goal
(see Fig. 1). This strategy
avoids lengthy searches in the case of small food sources.
|
|
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Training of Cataglyphis to feeding sites was according to standard procedures. In short, feeders were established at distances of 5 m, 10 m, 20 m, 40 m, 50 m, 60 m or 75 m to the north of the ant nest. Initially, and in order to attract the ants to the feeding site, a trail of biscuit crumbs was laid out towards the feeder. The feeder consisted of a Petri dish, 3 cm indiameter, glued into the lid of a jar, 7 cm in diameter. This arrangement prevented food items from being blown out of the feeder and thus contaminating the desert surroundings. Furthermore, it allowed removal of the feeder without leaving an odour mark on the desert floor. The feeder was filled with biscuit crumbs of selected size (sieved to roughly 2 mmdiameter). This promoted rapid and frequent visits to the feeder since the crumbs were small enough to be easily carried by foragers, and it reduced the number of (too small and lightweight) crumbs blown out of the feeder. For some experiments, ants were marked individually with a colour code (small dots of automobile varnish applied with insect pins to thorax and gaster).
Concentric circles were drawn around the feeding sites to facilitate recording of the ants' approach trajectories (indicated in Fig. 1). We noted the distance from the feeder at which the ants picked up the odour filaments and changed their courses, often quite abruptly, from a roughly tangential approach downwind of the feeder to a slightly zigzagging course directed upwind towards the feeding site (indicated as zigzag lines in Fig. 1). Along with this `downwind distance', termed d, we recorded the nest-feeder distance, the date and time of day, wind direction, wind speed and animal identification in those cases where the ants had been marked individually.
Ants change, and presumably optimise, their approach trajectory during
their initial visits to a familiar feeding site (see for example fig. 6 in
Wolf and Wehner, 2000). We,
therefore, waited for at least 1 day after the ants had been trained to a new
feeding site before we started to record their approach trajectories. It was
at least partly because of this gradual optimisation of approach trajectories
that the variance of the recorded downwind approach distances was almost as
large for any given individual ant as it was for different individuals (when
comparing their mean values). Therefore, we used all measurements of downwind
approach distances, irrespective of whether or not individual ants had
contributed more than one measurement, but did so only for the construction of
distribution diagrams (Fig. 4). For statistical analyses of significance levels and regression lines (e.g.
Fig. 5) we first averaged the
values obtained for any given individual and used the resulting mean values
for further (second order) statistical analyses. Hence, in all statistical
treatments, each ant contributed just a single datum point. Since unmarked
ants could not be differentiated they were regarded as a single individual for
the purpose of statistics. For our data set, this treatment reduced the
significance level of regression analyses and was thus regarded as
conservative. This was due to the (sometimes greatly) reduced number of
individuals (N), even though the variance of several individuals was
thus collapsed into a single datum. Statistical analyses were performed
according to Sachs (1992
) and
Sokal and Rohlf (1995
). In the
text below, N signifies the number of animals, and n the
number of measurements made.
|
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Wind speed
First, we examined the dependency of d on wind speed
(Fig. 2). In the Tunisian
desert near Maharès, wind speeds usually range from 3 to 6 m
s-1 (Fig. 2A). Lower
wind speeds occur regularly in the early morning, though mostly before
Cataglyphis starts to forage. At wind speeds around 8 m
s-1 locomotion of the ants becomes noticeably impaired, and towards
9 m s-1 the ants quit foraging.
|
Fig. 2B illustrates that d depends on wind speed only marginally, if at all. When data for all nest-feeder distances and all wind speeds are pooled, there is a small but significant negative slope of the resulting graph (-0.17, different from 0 with P<0.001; r2=0.0625). This means that at higher wind speeds, the ants appear to steer closer to the feeding site, presumably as the result of a smaller range of the odour plume and more turbulent air flow under these conditions.
However, the different wind speeds were not evenly spread among the different nest-feeder distances. In fact, the lower range of wind speeds prevailed during experiments where nest-feeder distances of 5 m and 10 m were examined. Considering the dependency of the downwind approach on nest-feeder distance (see below), this may have skewed the relationship depicted in Fig. 2B. We therefore analysed the data for the different nest-feeder distances separately. Fig. 2C shows the data sample collected for the 5 m nest-feeder distance. This experiment happened to cover the broadest range of wind speeds (1.2-8.7 m s-1), although there was no dependency of d on wind speed (slope=0.02, not different from 0 with P>0.1; r2=0.0025).
This observation prompted us to perform an analysis of covariance (ANCOVA;
see Sokal and Rohlf, 1995) to
differentiate the dependency of d on wind speed from that on
nest-feeder distance, D (see Fig.
5). Fig. 2D shows
the same data set as Fig. 2B -
pooled observations from all experiments - but the data were now corrected for
the dependency of d on D. It is immediately evident that the
small negative slope visible in Fig.
2B has disappeared completely, and no dependency of d on
wind speed is discernible. Not surprisingly, therefore, the analysis of
covariance did not yield a significant correlation either (P>0.1;
r2=0.0144).
We also tried to examine the influence of wind turbulence. A dense row of
pebbles was arranged perpendicular to the prevailing wind direction just
downwind of the feeding site. This should significantly alter turbulence close
to the desert floor (see also fig. 10 in
Wolf and Wehner, 2000) and
downwind of the feeder. Initially, the ants did not appear to alter their
downwind approach after this manipulation. However, they quickly recognized
the pebbles as landmarks and approached the end of the pebble row that was
closest to the nest. This prevented any meaningful continuation of this
experiment.
Wind direction
In our experimental area, wind patterns are remarkably reliable during the
summer. Eastern winds prevail at daytime, as illustrated in
Fig. 3A. Changes in wind
direction in the morning and late evening
(Wehner and Duelli, 1971) are
mostly irrelevant for the strictly diurnal Cataglyphis foragers. It
is mostly during unusual weather conditions, such as sand storms, that strong
winds blow from other directions during the day. However, Cataglyphis
does not forage under most of these conditions, that is, either under
completely overcast skies or at wind speeds exceeding 9 m s-1.
|
Details of the ants' approach trajectories may contribute to the
independence of d from wind direction. The ants approach a familiar
feeding station on idiosyncratic though more or less linear paths and aim at a
lateral (downwind) distance d that has probably been established in
the course of previous visits (Wolf and
Wehner, 2000). If the animals have not encountered the food odour
until they have reached a position where the feeder is roughly perpendicular
to their approach path, they often adopt a curved trajectory, centred, more or
less, on the feeder (Fig. 3C;
see also fig. 2 in Wolf and Wehner,
2000
). Hence, during the last part of their downwind approach, the
ants may keep an almost constant distance to the feeder until they pick up the
odour trail.
Nest-feeder distance
Different feeding sites were established at distances of 5 m to 75 m from
the nest (see Fig. 1). Beyond a
distance of about 20 m it became increasingly difficult to train ants to the
feeder. There were two reasons for this. First, the animals were reluctant to
travel such large distances at all. Instead, they searched for and exploited
other food items, such as small insect carcasses, on the way. Beyond 40 m this
was often true even if the ants had been familiar with the feeding site. The
risk of experimental animals being eaten by predators also increased
noticeably with larger nest-feeder distances. Second, ants from neighbouring
nests inevitably discovered the feeding stations, where they often proved more
numerous and competitively superior. As a consequence, the number of
observations gradually declined towards larger nest-feeder distances. In the
course of a week, only three ants could be trained to a nest-feeder distance
of 75 m, and they visited the feeder just six times.
The distributions of d values observed at the different feeding sites are presented, in histogram form, in Fig. 4. First, it is immediately apparent that the peak values (as well as the means) of the distributions consistently increase with increasing nest-feeder distances, D. On average, the ants' feeder approach distance, d, was larger the farther away from the nest the feeder was located. The corresponding relationship between downwind approach and nest-feeder distance is shown in Fig. 5A. This relationship proved linear with high significance. The best-fit regression line follows the term d=0.046D+0.56 (values in metres; slope different from 0 with P<0.0001, r2=0.7225, t=13.31). This translates into downwind angles steered by the ants when approaching the feeder of 3° to 8°.
This angular range of 3° to 8° results from the intercept (offset) of 0.56 m in the above equation. When the regression line is shifted down the ordinate to intersect it at zero, the resulting downwind angles average 3.0° over all nest-feeder distances (values for the actual feeders are 1.6° at 5 m, 3.1° at 10 m, 2.4° at 20 m, 3.1° at 40 m, 2.6° at 50 m, 2.7° at 60 m and 2.3° at 75 m).
Second, the distributions of d values becomes broader and the peak values lower, the larger the nest-feeder distances are. This is evident in Fig. 4, and is also indicated by the standard deviations depicted in Fig. 5A. This observation seems to indicate that the ants' navigation uncertainty increases with increasing distance of the goal. We therefore analysed the scatter of d in some more detail. Scatter values were calculated as the difference between a given measurement of downwind approach distance, d, and the mean of all d values for the particular nest-feeder distance, D (taken as absolutes; this measure is closely related to the standard deviation). This was done for the same data set as in Fig. 4, that is, for the pooled data from all trials (see Materials and methods; examining within-animal and between-animal scatter separately yielded similar results, not shown). Fig. 5B shows the relationship between the scatter of d and the nest-feeder distance, D. A trend line follows the term: scatterd=0.008D+0.443. A regression line was not determined since the data points are not normally distributed, partly because of the calculation procedure mentioned above. The angles subtended by the half-widths of the distributions decline from 9° to 2° as the nest-feeder distances increase from 5 m to 60 m (inset in Fig. 1 illustrates the distribution of approach distances in the experimental setting). These values agree surprisingly well with the downwind approach angles mentioned above. The scatter for the 40 m nest-feeder distance is exceptionally high, perhaps because of one particular experimental situation: just before this feeding site was established in 2002, a thunderstorm moistened the soil to a degree that the desert floor became slippery even for the ants. The soil took more than two weeks to dry to its previous surface structure.
Third, despite somewhat different conditions between the various experiments, the results were remarkably consistent. The particular situation for the 40 m nest-feeder distance has just been mentioned, and the large scatter in this experiment was the only notable exception to the otherwise observed consistency. Data for the 5 m, 10 m and 20 m nest-feeder distances were also collected in 2002 but with dry and sunny weather throughout. Nest-feeder distances of 50 m and beyond were examined in 2004.
Finally, the numbers of animals contributing to the distributions were quite different, ranging from more than 29 to three individuals (for detailed data see legend of Fig. 4).
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
We used this downwind approach behaviour to examine the orientation
strategy employed by the ants. In particular, we wanted to differentiate
between the `goal expansion' and the `error compensation' strategies outlined
in the Introduction (see Fig.
1). The major finding of the present study is the clear linear
relationship between the downwind distance, d, steered by the ants
when approaching a familiar feeder and the distance, D, between nest
and feeding site (Fig. 5A).
This is clear proof that Cataglyphis fortis ants employ an `error
compensation' strategy. Significant contribution of a `goal expansion'
strategy can be ruled out since the ants' behaviour - the downwind approach
distance, d - is independent of parameters affecting odour spread,
such as wind speed (Fig. 2), turbulence or wind direction (Fig.
3). This is the first demonstration of the use of an `error
compensation' strategy in animal navigation, whereas both `error compensation'
and `goal expansion' strategies are well-documented in human navigation
(Gladwin, 1975;
Lewis, 1994
).
In detail, the range of 3° to 8° that the ants have been observed to steer downwind of the direct course to the feeder might be interpreted as the ants' own assessment of their navigation uncertainty (see Introduction). This holds true when assuming that the animals optimise their approach under time and energy constraints. The optimal downwind angle should just exceed the ants' navigation uncertainty: a smaller angle, on the one hand, may occasionally lead the animals into the area upwind of the food source, that is, past the range of the odour plume. This would necessitate intensive searching for the food target. A larger downwind angle, on the other hand, would result in unnecessarily long approach trajectories.
For the sake of illustration let us assume that in the ant's path
integrator, the target (feeding site) is surrounded by a range of uncertainty
(Fig. 6, grey area). This
uncertainty range has a directional (angular) and a distance (linear)
component. And while these uncertainty components are most probably
symmetrical with regard to the goal, the search space produced by this
uncertainty range is polarised with respect to either component. This is due
to (i) the wind carrying the food odour in one direction only (polarisation of
the angular component), and (ii) foraging ants acquire strong sector
selectivity, that is, they eventually restrict their foraging to a narrow
sector of their nest surroundings within which they acquire and use
landmark-based route integration (linear component)
(Wehner, 1987;
Wehner et al., 2004
). To
reduce search time, the foraging ant should take advantage of this asymmetry
by heading towards the segment of search space (grey area in
Fig. 6) that contains maximal
information. In the case of the angular component, this is the downwind area
(as described in the present account), and in the case of the linear
component, this is the area closer to the starting point (the nest) and
familiar to the ant by previously acquired landmark information. As to the
latter aspect, it has indeed been observed that ants foraging within narrow
linear channels search within a near-target range that is closer to the
starting point rather than centred on the target itself
(Sommer and Wehner, 2004
).
Is this interpretation realistic? Indeed, are there other, preferably independent, ways to determine the ants' navigation uncertainty? There are several factors that indicate that it is realistic. First, the width of distributions of d values (Fig. 4, scatter of approach distances in Fig. 5B). The scatter of d values for a particular feeding site may be interpreted as a direct measure of the ants' navigation uncertainty, whatever the underlying causes (such as genuine navigation constraints of the ants, substrate structure, obstacles, etc.). Conspicuously, and in support of the above interpretation, the half widths of the distributions were in the range of 2° to 9° (see inset in Fig. 1 for an illustration of distribution of d values; regression line in Fig. 5B corresponds to 1-5°).
Second, the search density distributions of foragers returning to the nest
vary with their return distances. This has been demonstrated in experiments
where ants are intercepted on their return from an artificial feeder and
relocated to unfamiliar territory where they search for the nest entrance
(e.g. Müller and Wehner,
1994). The widths of the search density profiles should reflect
the expected navigation error since, at least initially, the ants should
concentrate their search on the area predicted by their assumed navigation
uncertainty. Nest-feeder distances of 0 m, 5 m, 15 m and 50 m were examined in
previous studies (L. Bernasconi, Y. Nieuwlands and R.W., unpublished data; see
also fig. 3.35 in Wehner,
1992
). At a distance of 0 m (the animals were caught on their
return right at the nest entrance) the half width of the search density
profile was about 2.2 m. This may correspond to the intercept of 0.56 m in the
equation describing the relationship of d on nest-feeder distance
(see Fig. 5A). When this offset
is subtracted from the (re-evaluated) half widths of the search density
distributions observed at 5 m, 15 m and 50 m, thecorresponding error angles
are 6°, 7° and 3°, respectively. These values are indeed in the
range to be expected if the ants' downwind angle reflected navigation
uncertainty.
Third, the standard deviations of Cataglyphis' actual return
paths, as reported in previous publications. Müller and Wehner
(1988) investigated systematic
navigation errors that occur when unilateral turns are imposed on the ants
during their outbound journey. These systematic errors shed light on the
underlying orientation algorithm that may in itself provide an idea about
navigation uncertainty (below). What is of interest in the present context is
the angular scatter of the return paths. Müller and Wehner
(1988
; fig. 2B therein) provide
standard deviations superimposed onto the systematic navigation errors. These
deviations average 9° (range 3° to 20°) if the ants can use
polarised skylight as a compass cue but have no landmarks to support
orientation. This is again close to the uncertainty angles mentioned
above.
Fourth, the angular navigation errors to be predicted from the path
integration algorithm just mentioned
(Müller and Wehner, 1988)
are difficult to determine in the context of realistic foraging situations.
The errors produced during turns usually cancel out in the course of a
foraging trip since right and left hand (or rather, tarsus) turns occur with
almost equal frequency (Wehner and Wehner,
1990
). The lower range of systematic errors, associated with
imposed turns of 60° to 90°, is between 6° and 9° (fig. 2 in
Müller and Wehner,
1988
).
In summary, the published data that allow a comparison with the present results support the interpretation that the downwind approach of Cataglyphis foragers actually reflects the ants' own assessment of their navigation uncertainty.
At present, the question of how the ants acquire a measure of navigation
uncertainty cannot be answered conclusively. It appears, however, that the
downwind approach is optimised in the course of the initial few visits of a
feeding site. The approach trajectory of individual ants often moves closer to
the feeder during these initial visits and stays fairly constant later on
(fig. 6 in Wolf and Wehner,
2000). This observation indicates that learning is involved in the
adjustment of the approach trajectory, although the criteria that govern
learning and therefore may define an optimal strategy remain unclear.
In conclusion, the results of the present study are in full accord with the assumption that foraging ants employ an `error compensation strategy'. That is, the animals are informed about the spatial extent and asymmetric structure of the uncertainty range surrounding their goal. Also, the ants adjust the angular and linear component of their goal-directed (outbound) vector in such a way that they hit that sector of the predicted uncertainty range that contains most navigational information.
The `error compensation strategy' employed by Cataglyphis ants is
just one element in a suite of behaviours used to deal with navigation
uncertainty. The systematic search initiated when the entrance is missed upon
return to the nest has already been mentioned (Introduction;
Wehner and Srinivasan, 1981;
Müller and Wehner, 1994
).
Similarly, when a feeding site is missed, a comparable search is performed,
although this one is centred on an area downwind of the food target
(Wolf and Wehner, 2000
). It
will be interesting to examine, in future studies, whether
Cataglyphis is able to quantitatively adapt its strategies in dealing
with navigation uncertainties to the environmental situation, such as terrain
familiarity or odour spread.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Gladwin, T. (1975). East is a Big Bird: Navigation and Logic on Puluwat Atoll. Cambridge, MA: Harvard University Press.
Lewis, D. (1994). We, The Navigators. Honolulu: University of Hawaii Press.
Linsenmair, K. E. (1973). Die Windorientierung laufender Insekten. Fortschr. Zool. 21, 59-79.[Medline]
Müller, M. and Wehner, R. (1988). Path
integration in desert ants, Cataglyphis fortis. Proc. Natl. Acad.
Sci. USA 85,5287
-5290.
Müller, M. and Wehner, R. (1994). The hidden spiral: systematic search and path integration in desert ants, Cataglyphis fortis. J. Comp. Physiol. A 175,525 -530.
Sachs, L. (1992). Angewandte Statistik, pp. 1-848. Berlin: Springer Verlag.
Sokal, R. R. and Rohlf, F. J. (1995).Biometry: The Principles and Practice of Statistics in Biological Research (3rd edn) . New York: W. H. Freeman & Co.
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.
Wehner, R. (1987). Spatial organization of foraging behavior in individually searching desert ants, Cataglyphis (Sahara desert) and Ocymyrmex (Namib desert). In From Individual to Collective Behavior in Social Insects (ed. J. M. Pasteels and J.-L. Deneubourg), pp. 15-42. Basel: Birkhäuser.
Wehner, R. (1992). Arthropods. In Animal Homing (ed. F. Papi), pp.45 -144. London: Chapman and Hall.
Wehner, R. (1996). Middle scale navigation: the
insect case. J. Exp. Biol.
199,125
-127.
Wehner, R. and Duelli, P. (1971). The spatial orientation of desert ants, Cataglyphis bicolor, before sunrise and after sunset. Experientia 27,1364 -1366.[CrossRef]
Wehner, R. and Srinivasan, M. V. (1981). Searching behaviour of desert ants, genus Cataglyphis (Formicidae, Hymenoptera). J. Comp. Physiol. 142,315 -338.[CrossRef]
Wehner, R. and Wehner, S. (1986). Path integration in desert ants. Approaching a long-standing puzzle in insect navigation. Monitore Zool. Ital. (NS) 20,309 -331.
Wehner, R. and Wehner, S. (1990). Insect navigation: use of maps or Ariadne's thread? Ethol. Ecol. Evol. 2,27 -48.
Wehner, R., Meier, C. and Zollikofer, C. (2004). The ontogeny of foraging behaviour in desert ants, Cataglyphis bicolor. Ecol. Entomol. 29,240 -250.[CrossRef]
Wolf, H. and Wehner, R. (2000). Pinpointing
food sources: olfactory and anemotactic orientation in desert ants,
Cataglyphis fortis. J. Exp. Biol.
203,857
-868.